PATTERN, NUMBER, VARIABILITY, AND TAXONOMICSIGNIFICANCE OF INTEGUMENTAL ORGANS

(SENSILLA AND GLANDULAR PORES) IN THE GENUSEUCALANUS (COPEPODA, CALANOIDA)

ABRAHAM FLEMINGERI

ABSTRACT

Methods for study of bilaterally symmetrical, serially homologous sets of integumental organscomprising hair, peg. and pit sensilla and the pores of integumental glands as well as theirnumber and distribution in the genus £I/C,,1<II1I/" are described.

A survey of these organs was carried out on geographically representative samples of the17 discrete populations I recognize as valid species in the genus. The survey concentrated onadult females, but smaller numbers of adult males and some younger copepodid stages werealso examined. Numbers and arrangement of these organs. estimates of variability. and theirrelationship to total length were established for each species. Phenetic similarity in integu­mental organ arrangement is shown to concur with other morphological features within thegenus. Comparison is also made between number and arrangement of integumental organsand the geographical relationships among the members in each species group. Several newspecies in the attenuatus group are described on the basis of integumental organs and geo­graphical distribution. A preliminary study of geographical variation in the circumglobal.broadly tropical species £ . .I'I/htenl/i.l' is used to estimate the general complexity of geneticcontrol and the use of these organs to study gene flow and population variability in plank­tonic species.

The integument of arthropods bears numerousorgans that fall into two general classes:sensory receptors or sensilla, and glands. Sen­silla are composed of one to several sensoryneurons and generally two accessory cells, thelatter forming the external features which maybe in the form of an outgrowth, Le., a hair, acone, or a peg, or an ingrowth such as a pit orplate organ with sensory cell bodies locatedunderneath (Laverack, 1969; Schneider, 1969;Stiirckow, 1970). The regular presence of sen­silla containing nerve fibers has been demon­strated histologically in a variety of differentcopepods (e.g., Fahrenbach, 1962; Elofsson,1971),

In terrestrial arthropods integumental glandsare highly variable in number, in distribution,and in morphological detail (Eisner and Mein­wald, 1966). I ntegumental glands describedfrom copepods tend to be rather simple sacs

I Scripps Institution of Oceanography, University ofCalifornia at San Diego, La Jolla. CA 92037.

Manuscripl accepled May 1'173FISHERY BULLETIN: VOL. 71. NO.4. 1'173.

underlying the integument and communicatewith the environment via a simple pore penetrat­ing the integument (e.g., Clarke et aI., 1962;Fahrenbach, 1962; Park, 1966).

On the body of copepods as in mystacocaridsand other arthropods, sensilla and glands are ingeneral distributed in bilaterally symmetricalpatterns that are somewhat redundant on suc­cessive body segments, i.e., they appear to beserially homologous (Sewell, 1929, 1932, 1947;Fahrenbach, 1962; Hessler, 1969). It is highlyprobable that chemical communication via integ­umental organs, a widespread means for ex­changing information among arthropods andvertebrates (e.g., cf. Johnston, Moulton, andTurk, 1970) is essential to copepods. Dioeciousand nonparthenogenetic copepods must locateand correctly identify a potential mate withoutvisual aids. This search and contact procedure ismediated by pheromones in Eurl/fell/om andcalled "mate-seeking behavior" (Katona, 1973).Moreover successful culmination of the matingact requires attachment of the spermatophore

965

that permits passage of the sperm into thefemale's seminal receptacles (Wolf. 1905; Neu­baUl'. 191:{; Heberer. IH:~2; Fahrenbach. 1962).

Integumental organ systems are used widelyin arthropod systematics. Indeed, in somegroups, as for example, mosquitoes, dependenceupon chaetotaxy is essential. A unique andparticularly interesting application devised topermit identification of the fossilized remainsof chydorid cladocerans in extinct lake sedi­ments utilizes the number, size, and arrange­ment of integumental pores (Frey, 1%9, IH62).

Despite repeated mention of integumentalorgans in the early copepod literature, attemptsto apply them to study of marine species arerare. Notable exceptions must include With's(1915) detailed accounts of the sensilla sur­rounding the oral region for a number of speciescollected in North Atlantic samples. Sewellshowed considerable interest in the generaldistribution of body integumental organs inplanktonic copepods. His observations made ona broad variety of species are presented inscattered notes, remarks, and illustrationswithin the context of his faunal studies onIndian Ocean calanoids (1H29, IH32, 1947).Unfortunately, the diminutiveness of theseorgans, Sewell's omission of methods for study,and a critical estimate of their reliability con­tributed to their neglect by subsequent workers.Two studies on bioluminescence in planktoniccopepods (David and Conover, 1961; Clarke etaI., 1962) call attention to the potential value ofluminescing integumental glands for identify­ing the species of living specimens.

Conventional taxonomic systems organizingdiversity among calanoid copepods are stronglydependent upon sexually modified structures ofthe adult (copepodid stage VI) sometimesassisted by nonsexual morphological or meristicfeatures in the adult condition, as for example,spination and setation of appendages, seg­mentation of appendages, and segmentation ofbody tagmata. These sources of diagnostic in­formation serve all hierarchial levels, species tofamily. Due to the nature of calanoid ontogeny,all of these structures assume their definitivestate only in sexually mature adults. Thus,juveniles lie outside of existing systems, malesand females are only rarely served by the same

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FISHERY BULLETIN: VOL. 71. NO.4

system, and genera that are relatively undistin­guished in sexually modified structures tend tobe "taxonomically difficult."

The primary purpose of this paper is todemonstrate the potential significance of sen­silla and the pores of integumental glands on thebody tagmata to the systematics and phylogenyof calanoid copepods. From a survey of theseorgans in the genus Ellca!illllls, their numbersand arrangements provide an objective basis forgrouping related species, for distinguishingbetween sibling species, for relating adults ofeither sex to their respective species despitethe elimination of other common charactersby sexual dimorphism, for aiding in the specificidentification of late immature copepods, and forthe determination of regionalized cohorts thatapparently lack unrestricted gene How withmorphologically similar cohorts in otherregi 0 ns.

REMARKS ON THE GENUSEUCALANUS DANA, 1853

Ellca!allllS is a universally familiar marinegenus of eucalanid copepods. It contains pri­mary consumers that form a conspicuous partof the epiplanktonic and uper mesoplankton inlow to middle latitudes; some of the species areprimarily oceanic, others are neritic. Within itshabitat many of the species tend to be amongthe most abundant and largest (adult totallength ranges from about 3 to 7 mm) of theregional copepod fauna. Since the inception ofthe genus for E. IIttl'lI/wt/IS (Dana, 1853), about25 nominal species have been proposed. Contri­butions by Giesbrecht (1892), Johnson (1938),and Vervoort (1946, 196:~) provide the frame­work for the genus and its taxa. The currentworld literature indicates 12 nominal speciesin active use. Two are represented by two sub­species each, yielding a total of 14 widelyaccepted taxa.

Though ElIl'ltil/lIlI.~ is a morphologically dis­tinctive genus and its species are widespreadand relatively abundant, frequent questions andconfusion about the validity and rank of itsnominal species and subspecies tarnish itsliteratun'. Difficulties with the identititation

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

of the species emanate largely from the absenceof distinctive sexually modified appendages,the few available meristic characters in setationand the widespread dependence of the existingtaxonomic system upon relatively subtle shapesand proportions of segments and tagmata un­supported by rigorous estimates of variability.Difficulties and inconsistencies associated withthe rank of the taxa in the genus Eucalauus,notably in the elongatus group, might be theproduct of several factors: e.g., the lack of accu­rate data on geographical distribution, uncer­tainties about the significance of morphologicaldifferences among the subspecies, the wide­spread lack of an adequate basis for viewing theplanktonic taxon in the perspective of a biologi­cal population.

For example, questions or expressed doubtschallenge the validity of separating E. pileatusfrom subcrassus, and the two have often beenconfused with monachus (Deevey, 1960; Grice,1962; Vervoort, 1963; Lang, 1965). Confusionabout subteuuis appears to trouble some(Fukase, 1957). Awareness of variation andtaxonomic complexity within the nominalspecies attenuatus has been noted frequently(Sewell, 1947; Tanaka, 1956; Brodsky, 1962;Lang, 1965; Park, 1968), and similar questionsmust be raised regarding dentatu8 (Fleminger,unpublished data). Finally, a point must bemade with regard to the elongatus complex.Three decades have passed since Johnson's(1938) perspicacious revision based on so fewdata, decades of increasing oceanographic activ­ity and the accumulation of geographical andmorphological observation on these commonforms. Considering our increased experiencesand understanding the logic of justification forthe general practice of regarding inermis asa full species but continuing the two subspeciesof elongatus and the two subspecies of bungiiescapes me. On the basis of both morphologyand geography the known similarities and dif­ferences between inermis and its two cognatesand those between the subspecies of each ofthese cognates are about equal.

As part of an unpublished doctoral disserta­tion, Lang (1965) presented a taxonomic reviewand study of the distribution of Eucalanus inthe Pacific Ocean based on plankton samples

from the Scripps Institution of OceanographyZooplankton Collections. Lang's data on theelongatus complex, published in 1967, contrib­uted appreciably to our knowledge of geo­graphical relationships among its populations.Though providing considefable evidence favor­ing extension of the revision initiated byJohnson (1938), his use of subspecies wasretained. Expressed dissatisfaction with separa­tion of pileatus and suberassus and the con­siderable variation encountered in attenu­atus s.l. were noted in the unpublished portionof Lang's dissertation.

My attempts to strengthen the E Ilealauussection of Lang's manuscript for publicationusing the material on hand to clarify unresolvedissues were unsuccessful. Two issues emerged:Resolution of the difficulties depended on 1)expanding geographical representation to en­compass the world ocean and 2) the need todevelop more reliable morphological charactersfor distinguishing the reproductively isolatedpopulations within the genus. As conditionspermitted, I gathered geographic records andspecimens of Ellcalanus in conjunction withglobal studies on other calanoid genera includ­ing ClausoealalLUs and Poutellina (Frost andFleminger, 1968; Fleminger and Hulsemann, inpress). In addition, I began to examine variousstructures of Eucalanus at relatively high mag­nifications (200 X to 600 X). Useful characterswere found in the female genital segment, es­pecially in the shape and arrangement of theseminal receptacles, and in the male fifth legs.For example, general similarities in the semi­nal receptacles provided a promising basis forphylogenetic groupings within the genus anda dependable means for separating at leastsome of the species of the pileatus group (Fig­ure 1).

In the course of my survey, distinctivepatterns in the distribution of integumentalorgans on the urosome became apparent. Recallof Sewell's (1947) use of these features to sup­port his separation of attenuatus and pseudat­tenuatus prompted development of proceduresdescribed below to map integumental organs ondorsal and lateral surfaces of all body segments.The results provided the means for separatingregional populations, species, and species

967

71 NO.4ETIN: VOL. .FISHERY BULL

025 mm I

a-e,g,i,k

0.5 mm I

I , I Pf, h, J, - I

IiiI I]q

E1; Or

'~J-jl

l~{p I IOmm

q - t

f

h

k

a

b

968

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

FIGURE I.-Genus £lIculuIIIIS. Genital segment, lateralview. female-a. slIb/CIII/;S (Downwind 28); b. IlIl/nOllU/I/S

(Monsoon II); c. eru.\·,I'/I.I' (Alusku 4-36); d. IOIlKicep.l'

(Monsoon 24); e. 1//oIIucilllS (Alusku 5-7); g. pi/cuI 11.1'

(Lusiad VII Freetown); i. ,ll/berussl/s (Lusiad II H-I);k. dCll/ull/s (Naga SIIA 61-198); I. e!OIlKOII/S (Naga SIIA61-127); m. hyulilll/s (TRANSPAC 10 B); n. illcrl/lis (Mud­dauber 137-1); o. bl/lIKii (TRANSPAC 65 B); p. ca/ifornicl/s

(5606 50.80); q. U/ll'IIJ/U/ll.\ (EASTROPAC A 207); r.scwclli (A/lUll/is 11-31-119); s. purki (Boreas 19); t. /uIIKUC

(Monsson 24). Anterior portion of head. lateral view.female-f. pi}('u/lI.I (Lusiad VII Freetown); h. sl/hcrassl/s

(Lusiad II H-I); j. dCIl/(1/I/., (N aga 61-198). The shadedareas indicate the extent of sperm in the seminal recep­tacle. Positions for stations mentioned are listed inSnyder and Fleminger (1965. 1972).

groups within the genus and concurred with theevidence derived from study of the seminalreceptacles. Greater appreciation of the repro­ductively isolated populations within Eucalanus(Table 1) also revealed the compelling need formuch additional work on finer details to com­plete a satisfactory account of each species. Thefour geographical forms of attenuatus s.l.require comparative study of conventional mor-

phologieal features in both sexes. Their geo­graphical distributions should be amplified byreexamination of the great number of recordsand sorted specimens now in hand recorded col­lectively under uttenuatu8 s.l.

Evidence of geographical variation in 8ub­telluis, described below, requires additionalstudy and should be examined in the context ofco-occurrence with its sibling congener, mucro­i1atu,~. Also, closer geographical scrutiny shouldbe made of other widely ranging species show­ing broadly neritic habitat preferences such ascraNNUN and pileatus. ,

Realization that the significance of integu­mental organs in copepods overshadows andholds more widespread interest than the genusEucalanus is the basis for presenting the sur­vey of sensilla and pores within the frameworkof an incomplete taxonomic review. Completingthe global account of Eucalanus first would im­pose a long and unnecessary delay. Based onseminal receptacles, geography, and integumen­tal organs, the essential diversity within thegenus is now unmistakably clear. Details still

TABLE I.-Author's provisional list of valid species and phylogenetic groupings comprising thegenus £1/('oluIIl/s. Summarized distribution and biogeographic assignment based on records confirmedby author.------------------------------------subtenuis group:

1. E. subtenuis Giesbrecht, 1888. Broadly Tropical, circumglobol1 in eutrophic oceanic waters; epiplanktonic.Figure ge.

2. E. mucronatus Giesbrecht, 1888. Tropical, Indian Ocean to western Pacific in equatorial circulation systems2;epiplanktonic. Figure 9d.

3. E. crassus Giesbrecht. 1888. Trapical·subtropical. circumglobol in eutrophic broadly neritic waters; epiplank.tonic. figure 9a.

4. E. Jongiceps Matthews, 1925. 80real-temperate, circumglobal, Southern Hemisphere West Wind Drift svstem(= Southern Ocean Transition zone); epiplanktonic? Figure 9b.

5. E. monachus Giesbrecht, 1888. Tropical-subtropical, Atlantic, broadlv neritic; subsurface epiplanktonic. Figure9c.

pileatus group:6. E. piJeatus Giesbrecht, 1888. Tropical-subtropical, circumglobal, coastol- neritic; epiplanktonic. Figure 110.7. E. subcrassus Giesbrecht, 1888. Tropical, Indo-Pacific, broadly neritic; epiplanktonic. Figure lIe.8. E. dentatus Scott, 1909. Tropical, Austral-Asian seas; coastal epiplanktonic. Figure llb.

elongatus group:9. E. elongatus (Dana, 1849). Tropical, Indian Ocean to western Pacific in equatorial circulationsj epiplanktonic?

Figure 13b.10. E. hyalinus (Claus, 1866). Tropical-subtropical, circumglobal especially in eutrophic, oxygenoted waters adja­

cent to boundary currents; deep epiplankton to upper mesoplankton. figure 13c.11. E. inermis Giesbrecht, 1892. Eastern Tropical Pacific in eutrophic, low oxygen water: deep 'epiplankton to

upper mesoplonkton. Figure 130.12. E. bungii Giesbrecht, 1892. Boreal-subpolar, North Pacific, and Bering Sea; epiplanktonic to upper mesoplanktonic.13 E. califomicus Johnson, 1938. Temperate, North Pacific. West Wind Drift svstem (= North Pacific Transition

zone); deep epiplanktonic to upper mesoplanktonic. Figure 13d.

attenuatus group:14. attenuatus (Dona, 1849). Tropical, Indo-Pacific equatorial circulation systems; epiplanktonic. Figure lSd.15. sewelli sp.n. Tropical-subtropical, circumgloboJ; epipJanktonic. Figure 15c.16. park; sp.n. Temperate, North Pacific, West Wind Drift system (= North Pacific Transition zone); deep epi­

planktonic to upper mesoplanktonic. Figure 150.17. langue sp.n. Temperate, circumglobal, Southern Ocean West Wind Drift system (= Southern Ocean Transition

zone); deep epiplanktonic and upper mesoplanktonic. Figure ISb.

1 Evidence of three regionalized populations: Eastern Tropical Pacific; Tropical Indian Ocean to westernTropical Pacific; Tropical Atlantic.

2 Two questionable records from Tropical Atlantic: Florida Current (Owre and Foyo, 1967) and Gulf ofMexico (Fleminger, unpublished data). Forehead pointed but basal segment of mandible with two setae.

969

FISHERY BULLETIN: VOL. 71, NO.4

TABl.E 2.-Adult female Fllm/ill/lI.l: collecting localities and numoers of specimens surveyed for sensilla and pores. Allsamples taken with open nets 1/2 m or larger in diameter at toe mouth and towed horizontally or ohliquely at epiplank­tonic dept hs.

Species

Cruise or ship Station latitude Longitude Date A 8 C 0 G H K M N 0 p Q

Afram 1

Almka2

Arctic Exped.Atfullfis 11-31:1

Azul IBoreas

Bureau ofSea Fisheries 4

CalCOFI 52065504570858076108

Capricorn

C/U//ll 60:\

Chinook

Circe

[)(((lI/(111f 11"'~)

Dodo VI

Downwind

EA5TROPAC

Eastropic

970

F-l 14°00'N4-36 23°31'N5-9 26°00'N11-5 29°07'N1310(4) 38°49'N15 24°42'N31 20 0 07'N33 19°21'N34 t8°35'N35 lZ054'N36 15°45'N43 08°08'N45 05°41'N46 04°09'N48 00056'N51 Ooo07'N74 29°11'580 26°20'5119 30 0 23'N122 35°12'N123 36°59'NF- 1 23°38'N19 41°57'N64 58°21 'N148 48°55'NF1832 34°02'5A2000 33°04'5A2003 33°05'590.280 33°28'N120.50 27°33'N144G.15 24°28'N137.30 25°20'NPT 18 22°31 'N27 03°30'531 06°31'532 or 58'S5 15°41'N9 19°52'N13 14°48'N15 12°58'N4 42°33'N8 40 0 28'NNT 3 22°28'NNT 8 lZ029'NNT11 05°11'NNT 14 08°28'NNT 15 07° 16'NNT 16 05°39'NNT 25 19"04'NNT 27 09°46'NNT 30 07°27'NNT 33 19°42'5Camero 3 26°28'5Om 2.75.63 11°00'536 06°05'N49 lO o 19'N54 10 0 23'N55 10° 14'N55·15 09°45'N60 11°58'N86 12°00'5198 46°25'520C 44°36'522A 40°39'524 34°30'528 27°08'5J 087 01°34'NA 207 13°23'582 08°00'N

17 C 30'W86°44'W87°32'W88°47'W

168°03'W49°42'W20 0 36'W16°52'W16°59'Wl7°20'WlZ045'W19°48'W21°29'W22°45'W25°20'W28°43'W40 0 06'W46°05'W64° l7'W67° 15'W68°50'W

109°36'W165°06'W168°57'E15Z055'E

lZ044'El7°16'E17°47'E

1l7°47'W115°52'W110 0 28'W112°45'W105°53'W121°54'W124°41'W124° 11'W64° 12'W69°57'W68°09'W73°34'W

162°09'W173°04'W177°21'E141°38'E123°58'E118°24'E115°20'E112°39'E8Z047'E83°31'E77°42'E63° 12'E46°04'E

110000'E49°53'E53° II'E51°43'E51° 19'E51 °3 1'E55° II'E55°55'E

123°38'W112°0B'W92°02'W79°30'W72°02'W

105°00'W126°00'W104°00'W

?24 Jon 5226 May 5230 May 5319 Jul 4719 Jon 6727 Jon 6728 Jon 6728 Jon 6728 Jon 6729 Jon 67

9 Feb 6711 Feb 6711 Feb 6712 Feb 6714 Feb 6712 Mar 6728 Mar 6730 Apr 67

2 May 672 May 675 5ep 622 Feb 66

15 Feb 6612 Mar 668 May 628 5ep 628 5ep 62

13 Jun 5218 Apr 5524 Aug 5710 Jul 5826 Aug 61

9 Feb 5313 Feb 5314 Feb5314 Jun 6516 Jun 6526 May 6628 May 6617 Jul 563 Aug 565 Apr 68

16 Apr 6820 Apr 6823 Apr 6824 Apr 6825 Apr 6817May6823 May 6827 May 6828 Aug 6829 5ep 6826 May 6316 Aug 6420 Aug 6422 Aug 6422 Aug 6423 Aug 6426 Aug 64

5 5ep 644 Dec 57

10 Dec 5717 Dec 5720 Dec 5731 Dec 5726 Feb 6719 Feb 679 Dec 55

4

7

5

25

5

2

75

22

4

2

27

2I

33

2

5

2

75

6

5

2

54

5

711

35

3

44

4

3

23

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

TARLE 2.-C'ulltinf{('d

Species ~

Cruise or ship Station latitude Longitude Date A 8 C 0 G H K M N 0 P Q

EI Golfo I I CN2 24°38'N 109°22W 14 Nov 63 2II COl 25°35'N 110014'W 17 Nov 63 1VI AN2 28°37'N 112°56W 25 Nov 63

EI Golfo II XIV 82D1 26°31'N 111°03'W 22 May 65EQUAPAC H2O 10°00'5 163°00'E 17 Aug 56

51 20043'N 158°27'W 21 Aug 56 5520 00051'N 167°14'W 29 Aug 56 10521 00002'N 166°59W 29 Aug 56 1523 01 °55'5 166°52'W 30 Aug 56 2

(1'/\('/).\'11(,;' G 1.24.63 15°31'5 110000'E 10 Feb 63 2G 1.28.63 21°26'5 110001'E 12 Feb 63 3G 1.29.63 23°10'5 l10000'E 12 Feb 63 2

Gill" 2·74 34°24'N 75°36'W 10 May 53 28·9 28°20'N 79°48'W 12 Sep 54 3

Lusiod II HI 01°16'N 103°52'E 28 Jun 62 6H7 06°58'N 79°50'E 28 Aug 62 329 05°02'N 53°01'E 31 Jul 6245 05°00'5 62°00'E 14 Aug 62 451 00°57'5 62°19'E 17 Aug 62

Lusiod V 46 00002'N 58°52'E 30 Mar 6~ 448 00°01'5 63°oo'E 1 Apr 6350 00°00' 67°02'E 2 Apr 63 454 00008'N 74°59'E 4 Apr 63 2 264 04°54'N 92°02'E 19 Apr 6394 02°01'N 53°02'E 5 May 63

Luslad VII 75 H 7 00°28'5 10051'W 4 Jul 63 6MWT 14 32°29'5 09°04'E 6 Jun 63 4MWT 19 31 ° 11 '5 00056'E 9 Jun 63 5MWT 79 00055'N 11°29'W 6 Jul 63Freetown 08°30'N 13° 17'W 11 Jul 63 3

Monsoon 7 09°11'5 127°33'E 22 Oct 60 2 29 13°19'5 109°35'E 7 Nov 60 211 11° 15'5 103°32'E 20 Nov 60 213 17°01'5 93°29'E 25 Nov 6022 37°50'5 85°22'E 26 Dec 60 2 224 39°18'5 119°51'E 9 Jan 61 2 226 64°11'5 165°56'W 13 Feb 6131 32°35'5 160056W 8 Mar 61

Nago 61·13 08° 18'N 104°42'E 13Jan61 461·124 10012'N 103°50'E 10 Feb 61 251061.107 09°19'N 103°58'E 10 Feb 61 4 4SllA 61·198 09°11'5 115°33'E 27 Mar 61 11 2 2511861.26803°20'5 127°21'E 26 Apr 61 2 1

NORPAC lH 45°58'N 134°22W 30 Aug 5524·42H 40026'N 146°37'W 21 Aug 55 6

Scan IV·l 33°49'N 139° 10'E 15 Jun 69 55hellbock 90 06°01'5 95°46'W 26 Jun 52

109 03°41'5 81°30W 4 Jul 52r, Washing/on 13 1l016'N 64° 10'W 2 Jon 66 6

TO·S8·1 (5cot) 35 09° 45'N 96°04W 7 May 58 4Transpac 108 38°22'N 141°23'W 31Jul53 3

32 B 52°29'N 176°09W 15 Aug 53 3648 46°54'N 153°55'E 15 5ep 53 1

Troll 40 31°IO'N 128°48'E 10 Apr 5545 A 31°17'N 137°29'E 12 Apr 5556 34°21'N 138°29'E 13 Apr 55 3

Zetes 14 39°00'N 154°58W 17 Jan 66 2

• Spe:ies code: A ('rUS.\IIS G "l'111at"S M l'ulif()rnicf'S8 !1)IlKiI'Ceps H \lIh('ras""", N "arkiC /1ltUW,'h,H I iner",;s 0 langueD ml/crlmaflls J eJollgllfllS P .\i'It't'lJiE suhtelltl;s K In'alifllls Q (If {('II IIuti I.'i

F pilea,"s L himgii

Unless identifled by footnotes the samples are from the Marine Invertebrate Collections of Scripps Institution of Oceanography.

I University of Rhode Island.:l National Marine Fisheries Service, Galveston laboratory.3 Woods Hole Oceanographic Institution.4 Bureau of Sea Fisheries, Cape Town, Republic of South Africa." Commonwealth ScientifiC and Industrial Research Organisation, Cronulla, Australia." National Marine Fisheries Service, Beaufort laboratory.

H71

remammg to be analyzed will not affect basicconclusions to be drawn about the sensilla andpores In EII(·u[u}l/(s. For purposes of this papernomenclatural recommendations have been lim­ited to an essential minimum. The species Irecognize are summarized in Table 1. Asidefrom the integumental organs and dorsal andlateral views of the body, description of othercharacters is restricted to a few basic features(Figure 1).

Functional significance aside, the diagnosticqualities of body patterns of pores and sensillashould be examined in the Copepoda on a broadfront.

MATERIALS AND METHODS

Systematic analysis of sensilla and pores wascarried out routinely on adult females of allEllca[alilis populations known to me (Table 1).Numbers of specimens and collecting localitiesare shown in Table 2. Sample size varied foreach species according to its geographical dis­tribution, the overall frequency of variation,number and arrangement of sensilla and pores,and the availability of specimens. The numberof regularly occurring pores and sensilla on thebody of a specimen is large, ranging from 80 to140 depending on the species, and their unvary­ing arrangement in strongly patterned, bi­laterally symmetrical arrays eliminated the needfor examining large numbers of specimens inall but one case. Specimens were selected atrandom from within each zooplankton sample,but collecting localities were deliberately chosento represent the known distribution of thespecies; i.e., as material on hand permittedrepresentative specimens of each species wereselected for examination from peripheral, inter­mediate, and central localities. Observations onadult males and on copepodite stages IV and Vwere also made on all species but were ordinari­ly limited to only two to four specimens each.

Sensilla and pores are exceedingly difficult toobserve in EIICU[UIIIIS using conventional lightmicroscopy without staining and clearingspecimens. Two simple methods were employedin this study. One served in examining generalexternal features of the various types of sensillaand their proximity to glandular pores. Speci-

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FISHERY BULLETIN: VOL. 71, NO.4

mens were immersed for about 24 h in a com­bined clearing agent and stain, consisting of 9parts lactic acid and 1 part of a 1% solution ofchlorazol black E (CBE) in 70% ethanol. Speci­mens were then transferred directly to a drop ofglycerol on a glass slide for microscopic exami­nation.

More intensive clearing is necessary foraccurate and systematic tabulation of body poresand sensilla. All tissue was removed from withinthe integument by heating specimens in a 10%aqueous KOH solution at 80 0 to 100°C for 2 to 4h. Rapid boiling should be avoided to preventthe integument from breaking apart. The ratioof KOH solution to specimens was about 50 ccper individual. The KOH digestion was re­peated using fresh solution if precipitates orfatty substances remained within the integu­ment. The concentration of KOH has been in­creased on occasion to 25% with satisfactoryresults. For ease in viewing during micro­scopic analysis, it is essential in preparing thespecimen to digest all tissues and eliminateprecipitates from within the integument.

Following digestion the empty, still intact,exoskeleton is prepared for staining by a rinsein distilled water for 1 to 2 min and transfer to70% ethanol for 1 to 2 min. These rinses shouldbe repeated if flocculent precipitates remainwithin the integument. I mmersion for about30 sec in a solution of 1% CBE dissolved in 70%ethanol stains specimens intensely. Stainingis terminated by flooding the preparation withdistilled water and transfer of the specimenthrough a brief rinse in water to a drop ofglycerol placed on a glass microscope slide forexamination. Stained specimens suspended inglycerol may be stored indefinitely in appro­priate slide storage boxes.

Washing and staining were carried out undera stereomicroscope using 3-spot deep depressionslides and with solutions changed with the aidof finely drawnout glass pipettes equipped withrubber bulbs. Sensilla are usually lost in thisprocess, leaving the stained cuticle puncturedby clear perforations. Glandular pores alsoappear as clear perforations permitting lightto stream through, but differ in shape andappearance of the margin as described below(p. 973).

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

Length measurements were carried out withthe aid of a stereomicroscope at 24 X and 40 X

magnifications depending on the size of thespecies. The microscope was equipped with amechanical stage and an eyepiece reticle bear­ing a ruled scale of 100 divisions. Total length(TL) was taken from the right lateral view intwo steps: one measurement along an imaginaryline extending from the anteriormost tip of theforehead to the dorsal most juncture betweenprosome and urosome (Fleminger, 1967) andthe second along an imaginary straight linefrom the dorsal most juncture of prosome andurosome to the posteriormost point on the rightfurcal ramus omitting the setae.

Examination of specimens for perforationnumber and distribution was carried out withthe aid of a compound microscope equipped witha mechanical stage at magnifications of 150 X

to 600 X. A camera lucida was used in thepreparation of drawings to approximate spatialarrangement of perforations in each form.

The outline drawing with perforations wasreproduced by electrostatic duplicating machinefor use on subsequent specimens of the speciesas a data recording form. Allowance was madefor small variations in the distance betweenregularly occupied perforation sites; all missingand additional perforations were recorded onthe form together with length measurements,sample. and specimen number. No attempt wasmade to estimate variability in the distancebetween adjacent perforations.

GENERAL OBSERVATIONS

Three general types of sensilla were found inEucalanu8 (Figures 2, 3). They resemble re­latively simple types found in other arthropods(e.g., see Snodgrass, 1935; Bullock and Hor­ridge, 1965; Schneider, 1969) and are as fol­lows:

1. Hair (trichodea) sensilla (Figure 2d);slender, elongated, uniformly attenuated, andunarmed; roughly 20 to 150j.l in length and 1to 5j.1 in diameter at the base; observed only onthoracic segments II to V.

2. Peg (basiconica) sensilla (Figure 2g); withpointed or rounded apex, ranging from 14 to

27j.1 in length, 1 to 3j.1 in diameter; they arewidely distributed over the prosome and usuallyoccur adjacent to the pore of an integumentalgland.

3. Pit (coeloconica) sensilla (Figure 2i):shallow circular depressions in the integument,3 to 6j.1 in diameter, the center raised in a nipple­like protuberance that stains intensively inCBE-Iactic acid; they were observed in fewspecies and only on the cephalon and anteriorthoracic segments.

As a rule the sensilla are lost during thecourse of tissue digestion and staining. Perfora­tions representing the sites of sensilla in pre­pared specimens appear under the light micro­scope as simple round openings. The innermostmargin stains noticeably lighter than thesurrounding integument. Large perforations(;:, 4fJ) from large hair sensilla may have acraterlike margin on the outer surface (Figure2e). Under the light microscope the walls of theperforation may slope to form a larger ellipticaloutline on the inner surface of the integument.Perforations derived from pegs are simple andabout 1 to 2j.1 across (Figure 2h). Perforationsderived from pit sensilla appear as a pair ofvery small openings separated by a slenderridge (Figure 2j). One or more of the threetypes of sensilla were found on all segments ofthe cephalon and thorax. One aesthetask-likesensillum, usually weakly plumose, is presentdistoventrally on the furcal rami in all species.No other sensilla were observed on the urosome.

The other class of cuticular perforations areformed by the ducts of underlying integumentalglands (Figure 2b). The glandular pore tendsto vary from a semicircular to a slitlike openingof 4 to 7j.1 across the maximum dimension whenviewed from above (Figure 2f-j). The marginstains as intensely as the surrounding cuticleand at least a section of the circumference turnsinward toward the underlying hypodermis.

My use of the term pore in connection withintegumental glands does not imply relation­ship to a different integumental feature, porecanals (Richards, 1951) discussed below.

Microscopic examination (300 X to 600 X

magnification) of intact specimens, especiallythose belonging to the elongatus group (treated

973

with CEE-lactic acid), frequently confirmed theconnection between the pore and a single, gland­like, gpherical to ovoid gac. roughly 30 to 75J.1across the maximum dimension (Figur 2b),and not unlike the glands noted in other cope­pod. (Fahrenbach, 1962; larke et aI., 1962:Park, 1966). Integumental glands may occuron all the segments of the body (Figure 3).

A notable featul'e of lhe perforations (bothsensilla and gland duct types) is their relation­ship to formation of the integument. Resemblingthat de. cribed in other arthropods (Dennell.1960), the exo. keleton in Ellca/(lIllls ha. beenobserved in the present study to consist of prismsapparently laid down over individual c lIs ofthe hypodermis. The prisms are joined by inter­prismatic septa presumably of secreted pro­cuticle that stains darker with CEE than thepri. ms. The organ-forming and neural cellextensions pas. between cells of the hypodermis.Hence passage of these featul'es through theintegument occurs in the interprismatic septa,a feature frequently observed in this study inall of the peci s. In specimens with w II dif­ferentiated prisms, numerous minute pel'fora­lions formed b~' the pore canals (-0.1 to 0.3J.1)ma~' be seen within each prism. As Dennell(1960, p. 461) states, perforations observed onthe surface ofthe cuticle formed by integumentalorgans and pore canals cannot b confused;the latter are numerous, minute, and withinthe margins of individual prisms; the formerare an order of magnitude larger and lie in thesepta between prisms. POI' canals were notconsidered in the analysis of Ellcaial/lls peJ'fora­tions.

LIMITATIO 5

Failure to obtain total elimination of tissueand precipitates in the hot alkali treatment andinsufficient stai ni ng were the commonest sou rcesof difficulties in carrying out microscopic exami­nation of the perforations. Specimens that hadmoulted hortly before fixation and species inwhich the exoskeleton is relati\'ely flabby (e.g ..species of the elongatus group) require greatercare in staining and handling.

Occa. ionally, areas of p rforation siz failto take up as much stain as the surrounding

974

FISHERY BULLETI ; VOL. 71. 0.4

a

I-rG RE 2.-Appcarancc of intact intcgumcntal organ.. andthc pcrforations Icft by thcse organs in the integument ofKOH-trcated specimens of ElIcalUlILIS .Hlblellll;S (adultfemalcs). Spccimens prepared for scanning clectron micro­scopc by Freon Critical-point drying, vacuum coatingwith gold-pallatllum and examined with thc aid of aCambridge Stcreoscan S.E.M. a. entirc spccimen in dorsalvicw: I mm ~ 24.4 II. b. schcmatic scctional view of typicalcombination of peg (basiconicum) sensillum and inte,gumental gland with pore. c. thorax in dorsal view: I mm:. 8.5 iJ.. d. hair llrichodeum) sensJllum: I mm = I /..I.

e. perforation in integument left by hair sensillum in KOH­treated specimen: I mm = 0.25 /..I. f. pore of integumentalgland: I mm = 0.25 /..I. g. typical arrangement of pego;en"lIum (right) and rorc (left). h. rerforati ns 111 intcgu­ment left by peg sensillum (right) and pore (left) in KOH­treated specimen. i. pit (coeloconkum) sensillum (left)and pore (right) of integumental gland. j. perforations inintegument Icft by pit sensillum (left) and pore (right) in

FLEMINGER: INTEGUMENTAL ORGA SIN GE US EUCALANUS

b c

9

.I

e

h

KOH-treated specimen. Figures g-j: cale, 1 mm = 0.5 /-I.

(Reference to trade names doe not imply endorsementby the National Marine Fisheries Service, NOAA.)

•I

975

FISHERY BULLETIN: VOL 71. NO.4

mm

A,~ 'd.- -.

FIGURE 3.-Distribution of sensillaand pores of integumental glandsin an adult female specimen ofE. suhtenuis; dorsal view on left,lateral view on right. Hair sensillaare shown as curving, attenuated,and varying in length; peg sen­silla are short, straight and blunt:pit sensilla are shown as an opencircle with a dot in the middle.Pore of integumental glandsshown as a half circle. Solid dotsrepresent perforation sites observedin specimen after KOH-CBE treat­ment and represent organs missedduring microscopic examinationof the specimen before digestionof tissues; intact specimen clearedin eBE-lactic acid solution for24 h prior to examination. Allorgans shown enlarged andschematically, though position isbased on records obtained fromcamera lucida drawings: micro­scopic examination carried out atmagnifications of from 150x to600x.

)

'l)

J

~0

\\

'. '. :

<::P "B00"D

O'l «)

0J Q:J0 .,p"cl 0

..,p ~'--/'

1), Q(~~

'"cP- "D0

'0"" '\ Ilk:,

~ d./

0

'ooJ ! q"

976

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

integument and appear as light spots that maybe mistaken for perforations. Direct compari­son with a true perforation is helpful to notethe reduced intensity of illumination passingthrough the light spot. Light spots tend to occurin the vicinity of usual perforation sites found inthe genus and may represent incomplete orarrested development of a gland or sensillum.Light spots were not recorded as perforations.

A number of perforations relatively difficultto observe were not examined systematically.They include the dorsal surface of the furcalrami and cephalolateral sites in the vicinity ofthe first and second maxillae and the maxilliped.The ventral surfaces of the prosome appear tohave few perforations but were not examinedsystematically.

DISTRIBUTION OFINTEGUMENTAL ORGANS

In each species the three types of sensillaand pores of integumental glands maintainessentially constant topographic relationshipsin arrangement and number on both the dorsaland lateral surfaces of the body, as seen for in­stance in subtelluis (Figure 3). One notablepattern appearing in all of the species for exam­ple is the distribution of dorsal hair sensilla,two appearing on the second thoracic segment,four on the third, and four on the fourth, thehairs always being arranged in transversesymmetrical rows, two hairs in each row (Fig­ure 3). Another type of persistent pattern isthe regular occurrence of the peg sensillumadjacent to the pore of an integumental gland(Figure 2). The organs are distributed in bi­laterally symmetrical patterns that exhibitserial homologies. Serial homology is indicatedby the partial to complete repetition of patternsin adjacent segments. As is shown below inthe account of the different species, the closerthe general morphological similarities betweenindividual pairs of species the more similar theoverall perforation patterns.

Every morphological type of sensillum orgland pore occupies a topographically uniqueposition, i.e., a designated site within the frame-

work of the overall bilaterally symmetricalpattern. The designated sites appear in KOH­treated specimens as morpholigically distinctiveperforations in the integument. Each body seg­ment has a constant number of organs (Table 3)arranged in a distinctive pattern that is repeat­ed with negligible variation within the series ofspecimens representing the species. Hence onan empirical basis the appearance of the sametype of perforation in approximately the sametopographic relationship in the series of spec­imens representing the species is compellingevidence that similarly positioned organs of thesame type are homologous among individualsof the same species. That is, they appear to bearthe morphogenetic relationships that are aprimary basis for regarding the same cephalicor thoracic appendage among individuals of apopulation as being homologous. Thus the ar­ray of regularly appearing integumental organs(designated sites) among the individuals of thespecies is assumed to comprise a homologousset characteristic of the species.

Among the species of a species group, integu­mental organs appearing in topographicallysimilar positions on the same body segment inall of the species are viewed as comprising ahomologous set characteristic of the speciesgroup. The integumental organs common tothe various species groups comprise the homo­logous set characterizing the genus. The implica­tion of phylogenetic redundancies is seen incomparing perforation patterns among thespecies (see Figures 9. 11, 13, 15) presentedbelow and in a segment-by-segment comparisonof the number of regularly appearing sites inthe species and species groups (see Table :3 andFigures 8, 9, 11, 13, 15).

In the case of a fused series of somites, i.e.,a tagma such as the cephalosome, the patternsare arranged in accord with the sets of bodyappendages in the tagma. The number of ho­mologous sites within the members of a speciesgroup is relatively high (cf. Figure 8 withFigures 9, 11, 13, 15) and the number of homol­ogous sites within the genus (55) is remarkablyhigh (Figure 6) considering that the speciesrange from a low of 83 sites in [ollgiceps to ahigh of 131 shared by III/ligh and ca/(fol'lIiclis(Table 3).

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FISHERY BULLETIN: VOL. 71. NO.4

TABLE 3.-Total number of lateral and dorsal perforation sites. by body and abdominal segments in ;:.80% of Eaca/ana."specimens examined. Body segments indicated by corresponding appendages.

Abdominal segmentsAnter iar body segments

Genus & species

Midbody segments-------=---- Abd Abd Abd Abd Grand

Al A2 Mnd Mx,' MX2' Mxp' PI Total P2 P3 P4 P5 Total 1 +2 3 4 5 Total total

EucaJanus:Number of homologous

sites in genus 8 6 4 4 4 29 5 6 6 19 2 5 53

subtenuis group:suhtenu;s111ucronat/H('rass"s/oI1R;ceps

l1IofWCl1l1.\

Number of homologoussites in group

12 68 68 68 68 6

8 6

10 106 68 66 66 6

6 6

44

4 17 63 14 18 15 34 9 43 12 14 13 34 5 37 11 13 13 34 5 35 11 13 13 34 5 35 13 15 13 3

4 5 35 I 1 13 13 3

51 642 640 440 544 5

40 4

22222

9978

10

7

12294848389

82

pi leotus group:pileufflS\u!Jerass""t!l'I1Il1(/{\

Number of homologoussites in group

elongatus group:e!onJ,:lllllshyaJinusin ennishunKi;('aliF)rflil'/ls

Number of homologoussites in group

8H8

8

1012141212

10

666

6

66666

6

666

6

48866

4

810 48 4

6 26 104 64 124 12

4

4 5 37 114 Y 47 154 9 45 15

4 5 37 11

8 7 43 716 9 67 912 11 61 716 15 71 1316 15 71 13

8 7 41 5

14 1418 1418 14

14 14

10 1011 1010 914 1214 12

7 9

333

44344

425050

42

3134294343

24

577

5

87488

4

244

44244

3 10I 123 14

8

4 174 16

94 174 17

1---

89109109

87

9111799

131131

72

aftenuatus group:1l1(enlllllliS

\('U'elli sp.n.parki sp.n.lanKa£' sp.n.Number of homologous

sites in group

12121212

12

6666

6

4444

4

6666

6

4 124 124 124 12

4 12

11 55 1311 55 1311 55 1311 55 13

11 55 13

16 1612 1212 1212 12

12 12

6644

4

51434141

41

8678

6

2233

2

755

10

17131521

II

123111111117

107

*Loterol perforation not counted.

VARIATION AT DESIGNATED SITES

As described above designated sites are thosetopographic positions on each segment occupiedby an integumental organ of a morphologicallyspecified type that occur within the context of arelatively fixed pattern on each segment. Thepattern on each segment is primarily character­istic of the species and includes elements charac­teristic of the species group and of the genus aswell.

No variation was (·bserved in the morphologi­cal nature of the organ occupying the designatedsite during occasional examination of randomlyselected intact specimens or in the characteristictype of perforation observed at the site in thesample of the species that was examined. Smalldifferences in the relative distance between adja-

978

cent sites within the pattern of a segment wereobserved frequently. They are negligible, how­ever, with respect to influencing the accuracy ofrecording details for each specimen. Replicatecounts of the same specimens taken on subse­quent days usually yielded similar results; thefew departures from zero variation rangedfrom 1 to ;3%. Spatial variation was not examinedclosely. Better understanding of its significanceshould be developed, as it probably reflectsindividual morphogenetic and possibly geneticdifferences.

Quantitative variation in terms of failure tofind a perforation at a designated site or findinga perforation in excess of the regular numbercharacterizing the segment (Table 3) is remark­ably low. To the extent that spatial variabilitydoes occur, it may be argued that the basic

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

scoring of individual perforations as represent­ing particular sites contains an element ofjudgment on the part of the observer.

Constant repetition of pattern (pel' !Jodysegment per species) in the distribution ofperforations (see Figures 9, 11, 13, 15) and thesmall amount of variation in the total numberof perforations observed in each species (Table4) indicate that personal judgment by an ex­perienced observer introduces negligible bias.The range about the mean number of perfora­tions per species (Table 4) does not exceed 10%with exception of slIbtellilis, a special caseactually representing three allopatric popula­tions occupying separate regions of the world'stropical belt. Indeed, perusal of Table 4 indi­cates that quantitative variation is not a simplefunction of either sample size or total numberof perforations.

With respect to presenting variation scoredfor each species, the frequency of a perforationappearing at each designated site is presentedsymbolically in three categories: sites occupiedin all specimens, sites represented in 80 to 99%of the specimens, and sites represented in 10 to79% of the specimens (see Figures 9,11,13,15).

TABLE 4.-Numher of localities. size of pooled sample. andnUI11ber of observed perforations in species of ElicaJUll11s.

Perforations

Species Localities Specimens Range

subtenuis group:

"'''{CHliisAtlantic Ocean 15 SO 125-141 134.8 3.2598I ndion Ocean 10 24 119-139 130.0 4.9111F-acific Ocean 10 36 114-135 123.6 4.9750

m/u.,.Of1{UI/S 6 20 86-91 89.4 1.5355eras.\".\ 4 11 83-85 84.0 0.4713fOllj.?iceps 4 12 79-83 827 1.1572monadlll.' 5 17 87-91 88.8 0.8106

pi leotus group:pilearlls 8 21 85-94 90.5 2.0384\lihcra.\.\llS 9 34 109-117 110.1 2.4722dente,'llis 5 24 109-115 1115 1.3313

elongatus group:

l'/oflKlllliS 11 19 90-101 94.9 3.3154II\'ali",o 14 25 109-121 114.8 3.2490111(,"111\ 7 16 94-106 99.7 2.7500h""1-:ii 5 15 127-133 1301 1.8086{'alUtlrtliew 6 23 125-135 131.2 2.1829

ottenuatus group:lItfenllalll' 16 26 117-126 122.0 2.0703H'wclli sp.n 24 43 107-113 110.3 1.2070parki sp.n. 5 18 109-114 111.s 1.3323lanJ.?(/(' sp.n. 7 14 115-121 117.6 I 7388

1500

--'

"5f-

"~ 1000

u

;;'!()

too 500

~:3E

1--9 10-19 20-29 30-39 40-49 50-59 60-69 70-79 BO-B9 90-99 100

OCCURENCE (%) OF PERFORATIONS AT DESIGNATED SITES IN Eucolonus

FIGURE 4.- Frequency of <l(currence of perforations atdesignated sites on the dorsal and right lateral integumentor !:'II ('<I 1<1 II lIS. The frequencies found in each species aregrouped in class intervals of 1O'il and each class is summedfor all species. Each designated site represents the occur­rence of a particular type of integumental organ appear­ing in a KOH-treated specimen as a distinctive perforationin the integument and occupying a topographicallyunique place within the framework of the overall bilateral­ly symmetrical pattern t(mnd in the species. For purposesor this graph the appearance of such a distinctively placedperforation in only one specimen of the pooled sample forthe species is sufficienI to include it among the number ofdesignated sites found in the species. Graph based onexamination of 448 adult female specimens representing17 species that yielded a total of 1,709 designated sites asdefined above.

Sites found in less than 10% of the sample have!Jeen omitted. A general summary of the vari­ability at each site is presented in Figure 4.Roughly 80% of the sites were represented by aperforation in every specimen. In 10% of thesites a perforation was observed in 80 to !)9%of the sample. The remaining 10% of the siteswere occupied at lower frequencies, !Jut thiscategory includes a number of sites that showremarkable patterns of geographical variationin .'; II/It I' //11 is that are discussed below.

Designated sites do not vary with respect totype of organ they represent, but one claSH ofvariation in topographic relationship is note­worthy. As mentioned above, peg sensillaregularly occur adjacent to the pore of an inte­gumental gland. The peg and pore pairing oftenvaried with respect to the position of the tworelative to the orientation of the segment. Thepeg tends to be lateral to the pore, but this maybe completely reversed or appear at any inter­mediate stage about a 360 0 arc. As a pair, how-

979

ever, they occupy a discrete position relativeto the remainder of the sites on the segment.This class of variation also deserves increasedattention as a potential fine scale indicator ofintrapopulation genetic variation.

Thus for application of integumental organsto copepod systematics at or above the rank ofspecies, variation encountered during this studyappears to be of no consequence. Moreover, theintraspecific variability observed may on thebasis of experience with SIlI)tl'llIli.~ provide adependable, measurable source for studyingpopulation homogeneity and gene flow.

PERFORATION SITESIN THE GENUS

Intra- and interspecific comparisons of per­foration number and arrangement are facili­tated by compelling evidence that sites similarin location and associated organ (i.e., glandpore or sensilla type) within and between speciesare homologous. Tables 3 and 4 and figures ofindividual species summarize the evidence thatin general perforation number and topographicarrangement are essentially constant andcharacteristic for each species. Further, all ofthe available observations indicate that thetype of organ found at any particular perfora­tion site is also constant.

As shown below, constant differences in num­bers and arrangement of perforations betweenthe morphologically more similar species aresmall. Quantitative and topographic differencesare correspondingly greater between speciesthat are more dissimilar morphologically (e.g.,Figures 9, 11, 13, 15). However, the total num­ber of perforation sites in the genus appears tobe about two times the number found in anyone species (Figure 5).

To construct Figure 5 an assessment of theextent of interspecific homology in sensilla andpores of Eucalal/us was obtained by rigorouscomparison of all the species segment by seg­ment. The tabulation was restricted to desig­nated sites, i.e., those occurring in 10% or moreof the specimens of each species. As describedabove, sites are judged to be homologous if theyoccur on the same segment in the same generalposition relative to the pattern characteristic

980

FISHERY BULLETIN: VOL. 71. NO.4

of the segment and represent the same kind oforgan (gland pore or type of sensilla). The placeof insertion of the segment's paired appendagesand the topographic position relative to theother sensilla and gland pores of the segmentaid in locating perforation sites. Overlaps ofcamera lucida sketches were also helpful whenallowance was made for relative and absolutedifferences in size. Allowance was also madefor small-scale variation of one or two perfora­tions relative to another one or a set as in pegand pore pairings; small differences in thespacing between adjacent sites and rotation ofone site relative to another was observed fre­quently within the general pattern arrangementof individual species.

The analysis reveals 163 different dorsal poreand sensilla sites and 30 lateral sites on eachside of the body. The total number of differentsites within the genus (223) is less than twicethat of the species with the highest individualscore (Table 3). Thus most sites in the genusappear to be common to many of the species andan appreciable number is common to all (Figure6).

Examination of small numbers of copepodidstages IV and V, adult males of all species and afew specimens of copepodid stage III indicatedconformity of each to the pattern characteristicof the species, except for segments that undergosexual modifications in the process of matura­tion.

PERFORATION NUMBERS ANDPATTERNS AMONG THE SPECIES

GROUPS

Interspecific comparison of the perforationsobserved in Ellcalal/u.~ is, as already mentionedabove, greatly simplified by the not unreasonableassumptions that repetitious similarities inpattern are dependent upon and a direct reflec­tion of genetic similarities. With this as aworking hypothesis, reducing and assimilatingthe distribution of perforation sites was enhancedby assembling similarities among the differentspecies and by using for comparisons all otherconstant topographic features of the integument.

All the species have in common 37 tergalsites, best seen in dorsal view and 9 pleural sites

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

a aAI b b AI

c c

A2a a

A2b ba a

Mnd b b Mnd

a a

MXI b b MXIa a

MX2MX2Mxp 00 00 00 00 00 00 00 00 Mxp

a a

Th I ... ..b Th I

b

a .. .. aTh II b b Th II

a aTh IIITh ill b b

ThN a a ThNb bTh :sl Th "Y..

Abd I - II a a Abd I - IIb b

Abd ill Abd illAbd N-:sl

a 1 a Abd TIl-""5l.b b

FIGURE 5.-Schematic presentation of all designated sites observed in adult female Eucalanl<s. Open-ended system fordesignating individual sites provided by abbreviations of appendages or abdominal segments together with row (a. b•... )and in dorsal view number to left or right of midline. or in lateral view number in dorsal to ventral order.

Cephalosome in Eucalanus contains the cephalon extending from the first antennae (A 1) to the second maxillae (Mx2).the maxillipedal somite (Mxp = ThO) and the first pedigerous somite (ThI). Thoracic segments ThIl. ThIll, ThIV bearingswimming legs 2. 3. and 4 are separate from one another. but ThV lacking a pair of swimming legs in the female is partiallyfused to ThIV. In the female abdomen the first two somites are fused (Abd.I-I1) during maturation of the genital segment.Abd.llI is separate and Abd.IV is separate in the elongatus species group but fused to Abd.V in the other three speciesgroups. The furcal rami are fused to Abd.V in all the species.

on each side. best seen in lateral view (Figure6). Tel'gal sites on the cephalmwme are poresand ,:)eg sensilla; on ThlI to ThV, all but two(ThlI-mb and Abd.IV-V-m) are hair sensilla;the two exceptions are pores. The pleural sitesof the cephalosome appear to include both poresand peg sensilla. Pleural sites on ThlI to ThIVare hair sensilla and those of the urosome arepores.

Within the genus four groupings may be dis­tinguished by virtue of additional perforations

that appear in common only among the speciescomprising each group (Figure 8). Additionalsupport for these groupings may be found inother morphological characters of taxonomicvalue in Ellcalallll.~ such as segmentation of theabdomen and the shape of the seminal recep­tacles in females (Figure I), fifth legs of adultmales, and various details in the appearance ofthe cephalosome. The groupings and theircomplement of species and geographical formsare listed in Table 1.

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FISHERY BULLETIN: VOL. 71, NO.4

gle of hair sensilla and a single medial siteslightly posterior to the anterior hair sensilla.The subtenuis group contains five generallyaccepted species that occur typically in eutroph­ic oceanic waters.

Sites in E, e1'aXx//x (Figure 9a) are identicalwith the pattern of the species group except thatthe perforations of row a on the mandibularsomitt~ are increased to two pairs (Mnd T-a-/l,/2 and rl, 1'2),

E. /o//g;eepx differs from the group patternsolely by the presence of a single mediodorsalsite on the genital segment (Figure 9b),

E, /ll1I//aelll/x (Figure 9c) differs from /lIlIrJi­

('epx in two features: the occurrence of a trans­verse row of three tergal sites across AbdJV-Vand three pleural sites on ThIl, ThIll, andThIV,

E. /llIlITII/wIIlX (Figure 9d) shows a smallincrease in the number of sites, On the cepha­losome up to six pairs of tergal sites may appearin addition to the group number between thesomite of the second maxilla and the maxilli­pedal somite, ThI shows an additional tergalpair on either side of the middorsal site, ThIIand ThIll have an additional site in the posteriorrow (ThI! T-b-/I and ThIll T-b-Il) to the left,but the symmetrical homologue to the right ofthe middorsal axis is absent. On the abdomenthe genital segment has two middorsal sitesand Abd,III may have one,

E, xllbtelllli,~ (Figure ge) has the largest num­ber of regular perforation sites in the genus,Dorsally, in addition to the species group num­ber, two more pairs appear in the somite of thesecond antenna, up to eight more pairs betweenthe somites of the first and second maxillae,four more pairs on the maxillipedal somite,four more pairs on Thl, and two more pairs onThIL ThIl and ThIll have a single asym­metrical tergal site (pore) within the quadrang­le formed by the hair sensilla as in III/IITII/III/IIX,

Laterally, ThIl and ThIll both show one ormore pairs on either side.

Within the group, xlI/III'll/lix shows the largestnumber of perforations (Figure 10) and themost extensive geographical distribution relativeto areal extent and sympatry (unpublished),Differenceg between x//lite 1111 i,~ and its clogegtcognate, 111/11'/'11 1/(/ III X, are concentrated in the

..... .

The Subtenuis Group

.' '.

Sites distingui:'\hing the subtenuis group(Figure 8c) appear on various portions of thecephalosome and thorax. On the cephalon themandibular somite bears two pairs of tergalsites. ThI shows only three sites arranged in atransverse row. ThIll and ThlV are :'\imilar,both being characterized by bilateral tergalpairs lying outside and anterior to the quadran-

FIGURE 6. - Designaled sites (represented by a dot) occur­ring at frequencies of "'" ROlfr within the pattern of eachspecies and present in every species of the genusEllcalanlls. Dorsal view on left, lateral view on right;outline of organism based on "lonKallls used solely asvehicle to show topographic relationships of sites.

982

t=:~jThTI P-rb-'l' -rb-4

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

(ThIT-o-(4 -(1 -o-r1 -r4

iThIT-b-(5 -(1 -mb -rl -r5

I .,

ThITTC:_~: ,:'jThIP-rb-l

ThIP-ro

-rb-2

FiGURE 7.--Schcmc for codifying dcsignated sites in F//cololl//I. Left. dorsal view of posterior portion of cephalosomeand thoracic segment 2. Right: lateral view of same.

I-irst unit of code for referring to a designated site is reference to the somite, using the appropriate appendage in thecase of the cephalosol11e or the hody segment (Thii. ThIll, .... Ahd.I-II. Ahd.IlI, .. J. Second unit indicates whetherit is dorsal. i.e .. tergal (Tl. or lateral. i.e .. pleural (Pl. Tergal sl'ls arc grouped in transverse rows. Thus, perforationsarc designated as heing on the right (r) or left (Il of the mid-sagittal plane and arc numhered frol11 the medialmost to thelateralmost (I. 2, ... j. Transverse rows are lettered in an anterior-to-posterior sequence (a, b, ...J. Perforations fallingon the midsagittal plane are tLTmed Illl'dial (111) and lettered in an antL'l'ior-lo-poslerior seqllellL'l' la, h, .. ,l.

Both right (r) and left (1) latcrial. i.c .. pleural <P>. sets afC ntllllhercd in a dorsal-tn-ventral sequence (1.2. .>. I:orconvenience <lntcrior-to-po"'lcrior division into rows lS utilized followin~ the corresponding set of tcrgal siles and art'also lettered in an anlcrior-!o-postL'l'ior sl'qllellL'e.

Various sites in dorsal and lateral views in the tlgurcs arc coditled <.!l:cording to the scheillc proposed ahove.

the tagma alRo Rhowing the mORt extenRiveg-eographical variation. Geographical variationin Sl/hlel//li.~ diRtinguiRhing the Indian, Atlantic,and East Pacific populations is diRcuRRed below(p. 999). The other four RpecieR fall within anarrow overlapping range (> 80 to < 95 perfora­tions). DifferenceR in number and arrangementeRpecially in the genital Regment characterizecmsslis and IIIIIcrollatl18, the two specieR over­lapping geographically in the Indian and WeRtPacific OceanR. DifferenceR in number and pat­tern alRo involving the genital Regment cliRtin­guish ('JYlSSIiS and /I//Illac/IIIS which co-occur inthe Atlantic Ocean. E. ('mS.~IIS alRo differsfrorr. //i/lfri('(pS. a temperate RpecieR of theSou:.hern HemiRphere, and from SIi/ill'/lIlis

in the Rites on the genital Regment.

The Pileatus Group

The pileatuR group (Figure 8d) conRiRtR ofthree Ribling RpecieR that are only weakly dif­ferentiated in general appearance from that ofthe RubtenuiR group. The pileatuR group alRo

strongly resembleR the RubtenuiR group in per­foration pattern, the primary differenceR beingin a small increase in the number of middorRalRites on the thoracic RegmentR. One additionalpail' occurR on the Romite of the firRt maxilla,and Ringle anterior middorsal Rites are foundon ThIll and ThIV. Three tergal RiteR mayappear on the genital Regment, but the pORteriortwo of the three RiteR are irregular in occurrencein pi/e(ltlls; therefore, at the RpecieR group level,the genital Regment iR beRt characterized by asingle middorRal site.

Among the individual RpecieR E. pi/eat/IS

iR eSRentially undifferentiated from the patternin the specieR grouJl (Figure lla). It lacks ter­gal RiteR on the Romite of the Recond maxilla andon Abel. III, although it haR three tergal RiteRacross Abd.IV-V. It alRo lackR pORterodorRalpleural sites on ThI, ThIl, and ThIll. The geni­tal segment may have one or two posterotergalRiteR in addition to the regular middorRal Rite.

E. deillat/is and .'!I/i('JYlSSIIS Rhare a number offeatureR that separate them from pi/mtl/s, name­ly two tergal pail'R of Rites on the Romitt' of the

~ ... .

.....

I, ,~

FISHERY BULLETIN: VOL. 71, NO.4

a

I .. ~

.... - ........

... ..

b

984

b

Imm

cd

FIGURE S.-Sites common to each spe­cies group of E/lcalan/lJ. From the left.3. elongatus group. b. attenuatus group,c. subtenuis group, d. pileatus group.A, dorsal view. H. right lateral view.

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

AImm

'- - ,

~ I

e

mm

b.'

B

FIGURE 9.-Species of the subtenuisgroup of Eucalanus: a. crassus, b. /"nRi­ceps, c. fnonachu.\'. d. mucronatus, e.sl/h/l'lIl/i.\. Dots represent sites occurringat a frequency of IOWI, in the pooledsample of the species; open circles aresites appearing in HO to 99'1, of thepooled sample: crosses are sites occupiedin from 10 to 79'1, of the pooled sample.Open triangles arc sites also visihle inlateral view but assigned to tergal sets.A, dorsal view. R, lateral view. Alltlgures of adult females made with theaid of a camera lucida.

985

EE~I-

5.0

4.0

3.0

WI

OJ

ElClnnoRo

FISHERY BULLETIN: VOL. 71. NO 4

omucronotusOlongicepsDmonochus0crossusIsubtenuis, Indian Ocean sampleosubtenuis, Pacific Ocean sampleIl] subtenuis, Atlantic Ocean sample

2.0 L-SL-0-'---9-L0-----"---10-'-0-L---L1110-~-12-'---0-~---'1~-0------'--14-,---10--'-----------'1boPERFORATION NUMBER

FIGURE 1O.-The subtenuis group of Flica/allll.l. Perforalion number plotted againsl lotal length (TL) in adult femalescomprising the pooled samples.

second maxilla, three tergal sites regularly onthe genital segment, two or more tergal sites onAbd.III, and, laterally, a pair of posterodorsalpleural sites on each side of segments Thl, ThII,and ThIll. E. tlelllllilis <Figure lIb) shows, inaddition, three tergal sites across Abd.IV-Vwhile SII/)(TIISSIIS (Figure lIe) has a single mid­dorsal site on Abd.IV-V.

As in the subtenuis group the species with

986

the most extensive geographical range, thecircumglobal pi/eo IliS, shows the most distinctivenumber of perforations within the species group(Figure 12). Differences between SII/)(,I'OSSIIS,

a broadly neritic species of the Indian and Paci­fic Oceans, and delllolllN, a coastal species ofAustral-Asian seas, are limited to arrangement,the number of perforations shown by the pooledsamples of the two species being equal.

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCA1ANUS

The Elongatus Group

Species of the elongatus group are charac­terized by 1 pleural and 23 tergal sites in addi­tion to the 37 and 9. respectively, present in thegenus (Figure 8a). The increase represents thesum of one pair in the forehead (A2T-a-11 and1'1). two pairs on the maxillipedal somite (MxpT­13, 14 and 1'3, 1'4), two pairs on the first free thor­acic segment (ThIT-11, 12 and 1'1, 1'2), one medialsite each on ThIll, ThIV, and ThV, two dorsalsites on the genital begment, and one additionalpleural site on each side of Th IV.

E. illf/'II/is (Figure 13a) is distinguished indorsal view by the following tergal sites: a setof eight on the Al somite, five on ThIV, three onThV, two on the genital segment, none on Abd.­III and Abd.IV, and three on Abd.V. In lateralview diagnostic pleural sites on either side in­clude one on the genital segment and none onAbd.IV.

E. dOI/,ljatl/s (Figure 13b) differs from eachof the other species in the group in a number ofdetails but only the two anterior tergal siteson the second antennal ~;omite (A2T-a-/1 and1'1 alld the tendency for more than two sites 011

Abd.III and Abd.IV are uniformly diagnosticwithin the group.

E. hYillill/iS (Figure 13c). Single tergal siteson ThI (ThIT-a-/1 and d) and the three tergalsites on the genital segment distinguish Iiyalilllisfrom the other species of the group.

E. ('alif(IJ'l/ic'I/,~ (Figure 13d). Sites that dis­tinguish cal ifill'll iCIIS from the preceding speciesare the pair middorsal on the somite of thesecond maxilla, the pair on the first free thora­cic segment (ThIIT-a-11, 12 and r1, 1'2), thepair flanking the median site on ThlI (ThIlT­b-/1, 12 and 1'1, 1'2), and in lateral view the threepleural sites on either side of ThIV. No consis­tent difference in number or in arrangement ofpedoration sites was found that distinguishescalifill'llil'lls from 1111I1,ljii. Both species are mor­phologically distinctive in other respects (e.g.,>,etation of the mandibular basis) and share acommon boundary across the North Pacific,clllUiil'lliclis occupying the temperate zone andhill/yii OCCUlTing to the north, without anyapparent evidence of i IItergTadatioll or hybrid­izatioll.

c

..'/,

~, e.

..

b

: :

~.. : ~ ..~.. .-

N' .(,\;

)N'

,

'" \

Imm

Imm

:..\

1" . ... \I o. \

A

B

FIGURE I I.-Species of the pileatus group of f;//('i//lI//II.I:

a. pi/ni/w, b. de//Ii/IttS, e.whercl.II//.I. Dots representsites occurring at a frequency of 100Ci( in the pooled sam­ple of the species; open circles are sill's appearing in 80 10

99r,.( of the pooled sample: crosses are sites occupied infrom 10 to 79';' of the pooled samplc. Opcn trianglcs arcsites also visible in lateral view but a~signed to lergal sCls.Dorsal view above, lateral view below. All figures of adultfemales madc with the aid of a camcra lucida.

987

FISHERY BULLETIN: VOL. 71. NO.4

3.0

EE~

...JI-

2.0

80

D subcrossus

• den/a/us

~ pi/eo/us

D

o

o

100

PERFORATION NUMBER

110

o

120

FIGURE 12.-The pileatus group of ElIca/al1I1S. Perforation number plotted against IOtal length (TL) in adult females com­prising the pooled samples.

As in the two preceding species groups a re­lationship between distinctiveness in overallnumber of perforations and geographical distri­bution is shown by the elongatus group (Figure14). The only circumglobal species of the group,hyalil/us, occupies a distinctive position withrespect to perforation number. The two speciesto the left, il/f'nnis and flollgatu.~, are geo­graphically isolated from one another and thetwo species to the right, bUl/gii and calijiirllicus,are biogeographically separated from one an­other. The distribution of hya/ilil/s in contrastbrings reproductively ripe individuals intocontact with all of the other species except bUI/­

gii (unpublished data).

The Attenuatus Group

Members of the attenuatus group have incommon 38 tergal and 8 pleural sites added to

988

the primary generic number (Figure 8b). Theincrease is widely dispersed about the body beingfound anteriorly on the second antennaI somite(A2T-a-/1, /2 and 1'1, 1'2), the somite of thesecond maxilla (Mx2T-ll, 12 and 1'1, 1'2) and onthe maxillipedal somite, where six pairs occur,two pairs more than in the elongatus group.Adding to the characterization are the anteriormiddorsal pail' of ThI, the six symmetricallyarranged tergal sites of ThV and the three tergalsites of Abd.IV-V. In lateral view pleural sitesare also more numerous, three pleural sites oneach side being found on ThIl, ThIll, ThlV,and on the genital segment. Every segmentexcept Abd.III bears more sites than the num­ber characterizing the genus, and the grouptotal of 109 sites is the largest among the fourgroups of species in Eucalal/us.

Four discrete populations of att(,ll/l((tll,~ s.l.emerge from the present study. They are mor-

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

• ..... 0

"

.1 '0.

......

Imm

.0 0""

~.. """( .. .... \)

b

--~-) C j

~\)

FIGURE B.-Species of theelongatus group of Eucalanus:a. inennis, b. e[onRQIllS, c.h.valilllis. d. californicus. Dotsrepresent sites occurring at afrequency of 100% in the pooledsample of the species; opencircles are sites appearing in80 to 99% of the pooled sample;crosses are sites occupied infrom 10 to 79% of the pooledsample. Open triangles are sitesalso visible in lateral view butassigned to tergal sets. Dorsalview above. lateral view below.All figures of adult femalesmade with the aid of a cameralucida.

B

a

Imm

m\

\;y)

\

989

ro bunrJli• califarnicus

80 0 inermiso hyalinuso elanqatus

o

FtSHERY BULLETIN: VOL 71. NO.4

ber and arrangement of designated sites isreadily available within the diagnosis for eachspecies.

EE..Jf-

7.0

60

50

o gO')

0080000

Omo 0

co 00

o 0

EJlcalanllS aUenllatlls (Dana, 1849),sensll stricto

(Figures lq, l5d, l8a, g, j, k, n, q)

E. ottCl/l/otl/S Dana, 1849, p. 18; 1853, p. 1080,PI. 75, Figs. 2a-d; Vervoort, 1946, p. 95-103(pars), Figs. 7a-c.

E. pseudattenuatus Sewell, 1947, p. 39, Test fig.7A. NEW SYNONYMY.

FIGURE l4.-The elongatus group of Eucalanus. Perfora­tion number plotted against total length (TL) in adult

.females comprising the pooled samples.

phologically distinguished primarily by thenumber and arrangement of integumentalorgans and biogeographically by inferred dis­tributions derived from the very different sets ofgeographical localities available for each form.In this regard it is important to stress that thesampling localities were chosen to representthe geographical extent of each population fromhundreds of localities of ottCl/l/otl/S s.1. obtainedduring the course of global studies on severalcalanoid genera. In the case of the two unusuallylarge species, parki and langae, the geographi­cal records represent all that are on hand. Amajor factor favoring separation of this complexinto four distinct species is the pattern seen inthe preceding three species groups and repeatedin the attenuatus group. That is, the specieswith the broadest geographical range also showsthe most distinctive number or arrangement ofsites, especially on the genital segment, andthat related allopatric species may show littleor no difference in these features.

In each instance the diagnosis is based on theadult female and stresses those designated sitescharacterizing the species within the group.Thus despite the more formal presentation andthe addition of non perforation data essentialto describe each species the information on num-

90 100 110 120

PERFORATION NUMBER

130 140 Diagnosis: Adult female: Characterized byhaving the largest number of designated sitesamong the species of the attenuatus group (Fi­gures 15d, 16; Tables 3, 4). Sites in additionto those of the species group include two pairs oftergal sites on ThIll (ThIIlT-b-ll, 12 and rI,r2), two similar tergal pairs on ThIV, two ter­gal sites on the genital segment, a single trans­verse row of three tergal sites on Abd.IV-Vand, laterally, three pleural sites on either sideof Abd.IV-V (Figure 15d). Length of triangularforehead extending beyond the lateral lobesoverlying the first antennae usually shorterthan width at origin, apex acute in lateral viewand not curving ventrad (Figure 15d). Mandi­bular basis with two setae.

Adult male: Thoracic tergal sites as in female.Abd.II with two tergal sites (Figure 18j).Mandibular basis with two setae. Foreheadweakly produced beyond base of rostrum, apexbroadly rounded in dorsal and lateral views(Figure 18g, k).

Additional description: Female lacking fifthpair of legs, abdomen with three separate seg­ments (Figure 15d). Male left fifth legs withfour segments, right leg about half as long andtrimerous (Figure 18q).

Total length: Adult female: range 3.63 to4.65 mm, mean = 4.10 mm, s = 0.2900, N = 28(Figure 16).

Adult male: range 2.93 to 3.50 mm, mean =3.135 mm, s = 0.1775, N = 7. Specimens select­ed at random from localities listed in Table 1.

990

'T1r'tTl~

Imm zC'ltTl?:'Z--ltTlC'lc::~tTlZ--l»r-0;:cC'l»z'"ZC'ltTlZc::'"t'lc::I"'l...r-...<:c::'"

~· .•... b

~ ,a

"e••••

Imm

..............

\

- .

I

A

......

~ ~ I

1,

I

FIGURE l5.-Species of the attenuatus group of El/cu!ul1l1.1: a. purki. b. '''''Rae. c. sewelli. d. u[(enuatus. Dots represent sites occurring at a frequency of1000/< in the pooled sample of the species; open circles are sites appearing in 80 to 990/< of the pooled sample; crosses are sites occupied in from 10 to 790/< ofthe pooled sample. Open triangles are sites also visible in lateral view but assigned to tergal sets. Dorsal view on left. lateral view on right. AU figures ofadult females made with the aid of a camera lucida.

FISHERY BULLETIN: VOL. 71 NO.4

EucdldrJUS sewel/i, n. sp.(Figures lr. ISc, ISb-d. o. r)

FIGURE 16.-The atlenuatus group of Eucu!unus. Perfora­tion number plotled against total length (TL) in adultfemales comprising the pooled samples.

E. attenuatas: Vervoort 1946, p. 95-103 (pars),Figs. 7d-f; Sewell, 1947, p. 39, Text-fig. 7B;Brodsky 1962, p. 113, Fig. 14.

¢ langae<> park!oattenuatusosewell!, Indo-Pacific sample• sewelll~ Atlantic sample

100

5.0

7.0

6.0

4.0

8.0

EE

--.JI-

Brodsky's (1962) description of pseudattenu­at as may be based on attenuatus s.s., but thefigures fail to provide adequate details of theforehead and the absence of information on dor­sal integumental organs on ThIll and ThIVleave the issue open.

Renlllrks: Dana's (1849, p. 18, 19) first local­ity given for attenuatus is from the vicinity ofthe Kingsmill ( = Gilbert) Islands in the westernPacific (13 April 1841). Other U.S. ExploringExpedition localities include the China Sea atabout lat. 5° to looN (15 February 1842) andthe Sulu Sea (2 February and 2 March 1842).All of these localities lie in Indo-Pacific tropicalwaters, the biogeographical zone and the geo­graphical region that yielded most of the recordsof attenuatus s.s. Moreover, Dana's figures(1853, Figure 2d, e) of attell/wtlls, while crudeemphasize a short wide-angled forehead charac­teristic of the tropical population.

Vervoort (1946) noted two morphologicalkinds of attell/wtll.~ s.1. in Sllellill.~ collections,and his illustration (Figure 7c) probably refersto attenaut us s.s.

Sewell's (1947) description of pseudattenuatusshows a pattern of integumental organs ascrib­able to the tropical species attenuatus s.s. Hisillustration of attenuatus (1947, Text Figure7B) appears on the basis of an incompleteaccount of integumental organs and the fore­head to be referrable to sewelli described below.

Geographical distribution: Verified localities(Figure 17) suggests a broadly tropical distri­bution restricted to the Indian and PacificOceans. A deliberate search among severalhundred plankton samples from Atlantic Oceanlocalities scattered over the lower latitudesfailed to yield a single specimen of attenuatuss.s. The species is widespread in tropical lati­tudes of the Indo-Pacific but appears to be mostabundant immediately downstream of eutrophicregions along the equator.

R(!i'1'enee: Three lots of reference specimensdeposited in the U.S. National Museum(USNM).

2 99. USNM 143848. Cruise Dodo VI, stn49, 1-m net, 0-200 m wire out (MWO); 20 Aug.1964,1445-1500 h; 10° 19'N, 53° ll'E.

399. USNM 143849. Cruise Dodo VI, stn 47,1-m net, 0-200 MWO; 19 Aug. 1964, 1825-1840h; 8°53'N, 53°09'E.

1 9. USNM 143850. Cruise Scot (T058-1),stn 35, 1-m net, surface; 7 May 1958,0343 h;9°45'N,96°04'W.

992

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

~rO_'~~~;;;;60_'__..,.....-""-..,.......:;0'-·..,......=;20'--· -":6o'-. -"'�o~O· -'.:"~0· _"18~0·--_-',.~0::...· __---'I~OO::..·~~----'160·

O'

o•o

140·180·IOO~

E ottenuotus group

~F~I~~~ t:

o g~~;Z~ (from Pork. 1968) ?C>~park! (from Long. 1965 ) • ~

o/anqae .'-.Ianqae (from Lang. 1965 ).. Ianqae (from Bradford. 1970) . . .. ' .'esewell!6affenuafus

20'

e

•

20'

60'

40'

FIGURE 17.-Gcographical localities of the species in the attenuatus group. All identifications except those of Park(l9hH) and Bradford (1970) verified by examination of integumental organs.

Diag lIo.~is: Adult female with mandibularbasis bearing two setae as in attelluatus. Differsfrom attelluatas in designated sites on ThIlland ThlV, each of which lacks the two pairs oftergal sites enclosed by the outer arc of sixtergal sites (Figure 15c). Genital segment lack­ing integumental organs. Abd.IV-V with twotransverse tergal rows and lacking pleuralsites (Figure 15c).

Adult male: Tergal sites on ThIll and ThlVas in female. Abd.II lacking dorsal integumentalorgans (Figure 18i). Mandibular basis with twosetae.

Additiollal descriptioll: Adult female withforehead more strongly attenuated and longerthan that in attellitatus (Figure 15c), apexusually curving weakly ventrad (Figure 18c).In relatively eutrophic regions of the I ndo­Pacific attn/lwtns and sewelli may co-occur and

resemble one another in size and general mor­phology, but differences in integumental organspersist. In strongly eutrophic tropical regionssewelli may exceed 6 mm in TL and exhibita more prominent conical forehead with roundedapex (Figure 18d). Male with fifth pair of legsas in attelluatlls (Figure 180, r).

Total lellgth: Adult female: range 3.89 to6.10 mm, mean = 4.720 mm, s = 0.6350,N = 43 (Figure 16).

Adult male: range 2.89 to 4.58 mm, mean =3.195 mm, s = 0.4680, N = 14. Specimensselected at random from localities listed inTable 1.

Geographica I distributio II: Verified localities(Figure 17) indicate a circumglobal range ineutrophic tropical and subtropical waters ex­tending to the subtropical convergences.

993

FISHERY BULLETIN: VOL. 71, NO.4

a b ~c d

fh

--........ 0'/

) \9 ---------....

--........--...

-------=:)k ~___.----/'---------" )---;~~~ //' ~/

( <rrrr? ~lfrr~ Vs ,-JJ~

O.5mm ~~~FIGURE 18.-Anterior portion of head. lateral view, female; a. Ell ("(/1(/11 11.1' (llIeI1l/{III1S (EQUAPAC S 21); b. sewell' (AI(lska

5-9); c. sewelli (Naga SIIA 61-198); d. sl.'welli (CaICOFI 5708 144.G 15); e. p(/rk' (Boreas 19). Anterior portion ofhead, dorsal view, male; f. parki (Zetes 14); ~. (l1I1.'11l1U[W· (EQUAPAC S 21). Anterior of head, ventral view, female; h.lal1gae (Lusiad 14). ThIV-V and abdomen, dorsal view, male; i . .1'1''''1'11' (CaICOFI 5708 144.G 15); j. a/ll'nlW[IIS

(EQUAPAC S 21). Anterior ponion of head, lateral view, male; k. allel//w[IIS (EQUAPAC S 21); I. park' (Zetes 14).Anal segment and fused furcal rami. dorsal view, male; 111. park' (Zetes 14); n. (//lel/llall[S (Monsoon 24). Fifth pairof legs, male, right lateral view; II. se"'('11i (CaICOFI 5708 144.G 15); p. 1(ll/g(le (Lusiad VII MWT 19); q. allel1l/{illlS

(EQUAPAC S 21); p. sewelli (Alaska 5-9); s. park' (CaICOFI 580480.130); left lateral view; t. park' (Boreas 19). Positionsfor stations mentioned are listed in Snyder and Fleminger (1965, 1972).

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

Types alld type locality: Holotype: 9. USNM143844. Cruise Downwind, stn 23a, 45-cm net,0-352 m; 19 Oct. 1957, 0000-0100 h; 38°46'S,83°20'W.

Reference: 399. USNM 143845. Cruise Down­wind, stn 28, 1-m net, 0-283 m; 31 Dec. 1957,0520-0542 h; 27°08.5'S, 72°02'W.

3 99. USNM 143846. Cruise Atlantis II-13,stn 8, 3;4-m net, depth'? 5 Oct. 1964, 1410-1435h; 41 °26'N, 55°45'W.

1 9. USNM 143847. Cruise Dodo VI, stn 55,1-m net, 0-200 MWO; 22 Aug. 1964, 1845-1858h; 10° 14'N, 51 ° 19'E.

Remarks: Brodsky's (1962, p. 113) record of(?) attenuatus appears from his illustration(Figure 14) and the locality off northern Japanto be referable to se /Celli. Other records thatappear to be assignable to se welli include Tanaka(1956, p. 266, Figure 4a), Ramirez (1969), andRoe (1972). This species is named to honor R. B.Seymour Sewell who among his many signifi­cant contributions to the copepod literatureinspired study of their integumental organsand directed attention to the complexity exist­ing in the attenuatus group.

E/lCatal1/1J parki, n. sp.(Figures Is, ISa. 18e, f, I, m s, t)

E. attelluatus: Park 1968, p. 533, PI. I, Figs.16, 17, PI. 2, Figs. 1-16, PI. 3, Figs. 1-13,large form only.

Diagnosis: Adult female: Mandibular basiswith four setae. Sites of integumental organssimilar to those of seloelli except for presenceof one medial tergal site on both the genitalsegment and on Abd.III, one or more pleuralsites on Abd.IV-V, and only one transven~e

tergal row on Abd.IV-V (Figure 15a).Adult male: Forehead prominent, protruding

as an elongate triangle about twice as far be­yond base of rostrum as in scwelli and attclIlI­otl/.~ (Figure 18£). Integumental organs oncephalosome and thorax as in female; Abd.IIwith or without one tergal site (in 11 specimens,6 with and 5 without). Mandibular basis usuallywith four setae, one specimen in 11 with threesetae.

Additiol/al desc1'iptiol/: Adult female withconical forehead and rounded apex as in Figure18e, differs from typical acutely pointed fore­head of se welli.

Totollel/gth: Adult female: range 6.40 to 7.17mm, mean = 6.744 mm, S = 0.1982, N = 18(Figure 16).

Adult male: range 5.20 to 5.96 mm, mean =

5.620 mm, s = 0.2380, N = 10. Localities ofspecimens listed in Table I, pooled samplerepresents all adults on hand.

Gcographical distributiol/: All records (Fig­ure 17) are from the North Pacific Ocean. Mostfall within the Transition zone (Brinton, 1962,p. 202) but a number also appear along long.155°W extending south to lat. 32°N, followingthe line of division between western and easternNorth Pacific Central Water (Sverdrup, Flem­ing, and Johnson, 1942, Figure 209A) which issupported by the relative elevation of the iso­therms in the upper 200 m of the mid-latitudesin the North Pacific relative to those of theSouth Pacific (Reid, 1965, Figure 2).

Types alld typl' IO('(flity: Holotype: 9. USNM143841. Cruise Norpac H5508, stn 24-42, 1-mnet, 0-200 MWO; 21 Aug. 1955; 1556-1610PST; 40 0 26'N, 146°37'W.

Reference: 1 9, specimen no. 2. USNM143842. Cruise Norpac H5508, stn 24 (up), 1-mnet, 0-200 MWO; 25 Aug. 1955, 1620 PST;42° 17'N, 146° 16'W.

1 9, specimen no. 1. USNM 14384:~. CruiseNorpac H5508. stn 25 (up), 1-m net, 0-200MWO; 25 Aug. 1955, 1816-18:n PST; 42° 17'N,150 0 00'W.

Remarks: Large forms of attel/uotus s.1. havebeen noted from the North Pacific by severalauthors (e.g., Tanaka, 1956, p. 266, Figure 4b;Lang, 1965 Park, 1968). Park (1968) fullyappreciating its distinctiveness described it indetail. He relinquished his original intention ofnaming it as a distinct species upon my recom­mendation, which was based on the apparentlyextensive variabi lity generally thought to pre­vail in Eucolal/us. At that time there was noreliable basis for distinguishing genetic fromphenetic variation and reliable capture records

995

were insufficient to provide an indication ofbiogeographical affinities. It is a great pleasureto name this species for TaiSoo Park in recog­nition of his acumen and farsightedness injudging copepod systematics.

EllCl1ll1nllS ll1ngde, n. sp.

(Figures It, ISb. 18h, p)

E. attenuatus: Bradford 1970, p. 353, Figs. 6-9.

Diagnosis: Adult female: Closely resemblingparki in size and appearance including theoccurrence of four setae on the mandibularbasis. Integumental organs as in parki except forsignificant increase in abdomen (Figure 15b).Genital segment and Abd.III each with two ter­gal sites. Anal segment (Abd.IV-V) with twotransverse rows of tergal sites as well as moreregularly occupied pleural sites occurring incopepodid stage V and in adults (Figure 19,Table 5), the mean total number being abouttwice that of parki.

10

FtSHERY BULLETIN: VOL. 71, NO.4

Additional description: Adult male: Integu­mental organs of cephalosome and thorax as infemale; Abd.II with two tergal sites as in geni­tal segment of female.

Total length: Adult female: range 6.44 to7.22 mm, mean = 6.847 mm, s = 0.2235, N= 14(Figure 16).

Adult male: 6.12 mm and 6.59 mm. Locali­ties of specimens given in Table 1.

Geographical distribution: Available records(Figure 17) indicate that langae is a resident ofthe circumglobal Transition zone in the SouthernHemisphere.

Type.~ and type locality: Holotype: 9. USNM143839. Cruise Lusiad VII, stn 14, Isaacs-Kiddmidwater trawl; 0-3,400 m; 6 June 1963, 1530­2300 h; 32° 30'S, 9°04'E to 32°24'S, 8°25'E.

Reference: 2 n, specimens no. 4 and 6. USNM143840. Cruise Monsoon, stn 18, Isaacs-Kiddmidwater trawl; 0-2,723 m; 11 Mar. 1961.2046-0303 h; 25 0 52'S, 155 0 44'W to 25 0 40'S,155°34'W.

Perforations

FIGURE 19.-Frequency distribution of the total number ofperforations on the anal segment (Abd.lV-V) in stage Vfemale copepodids above and in adult females below.Diagonal hashing represents Euca/anus parki, dotted arearepresents £. lanKa".

5

10

5

o

o

10 12

12

Remarks: Lang (1965) found specimens ofthis species at several Monsoon and Downwindstations (Figure 17) and noted their resemblanceto their North Pacific temperate cognate. Brad­ford (1970) also noted this similarity in record­ing it from off the Kaikoura Peninsula, NewZealand, and referring to Tanaka's (1956)mention of a large attel/uatus s.l. off Japan.

Though data on designated sites are lackingfor Bradford's specimens, the probability thatthey are referable to langae is sufficiently greatto include them under the species without re­servation.

Assignment of the sibling populations langaeand parki to separate species is based on twolines of evidence: 1) significant differences indesignated sites involving abdominal segmentsthat undergo modification with sexual matura­tion (Table 5, Figure 19); 2) apparent restric­tion of each population to temperate zones inopposite hemispheres (Figure 17).

Although data on actual depth distributionare unavailable for either species, most of the

996

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

TABLE 5.-Number of perforations on anal segment of parki and la/lKa(' in copepodid stage V andadult females of E/lca/a/l/ls.

Species Range \' N P

parki: stage « 0-5 1.75 1.4368 32adult'" 2-6 3.7222 1.2744 18

!unRue: stage V)' 3-9 6.1428 1.6036 28adult'" 6-12 8.1428 1.6576 14

Comparison of sample means of female specimens

park; stage V and adult'" 50 4.85 <0.001JWl~ae stage V and adult9 42 3.76 <0.001stage V: park; and la11KU(' 60 11.193 <0.001adults: park; and lanKae 32 8.55 <0.001

records of la 1/ ga I' and parki (Table 1) are basedon relatively shallow tows with open nets from300 m or less to the surface. Following theshortest prevailing surface circulation in thePacific Ocean, shallow water passage from thetemperate zone of one hemisphere to that ofthe other is at least 9,000 miles long. It wouldbegin necessarily in the eastern boundary cur­rents and continue in the equatorial circulationwhere crossover to the succeeding westernboundary current in the opposite hemispheremight occur. Assuming a high rate of 1 knotand an unrealistic expectation of continuousand direct transport would require a transittime exceeding 1 yr.

Among my unpublished records of attel/uatu.~

s.l. neither la I/gae- nor parki-like individualsof any copepodid stage appear in the equatoriallocalities (cf. Fleminger and Hulsemann, 1973,for geographical distribution of samples thathave been examined for Eucalal/us). Moreover,no specimens that might be attributable tolal/gae or parki on the basis of unusually largesize appear among the published records ofattel/uatus s.l. collected from the vicinity ofthe Pacific's equatorial circulation.

Transhemispheric passage at subsurfacedepths would be at transport rates that areprobably an order of magnitude less than sur­face transport. Evidence of tropical submer­gence by attel/uatus s.l. is lacking, however,despite widespread studies on the vertical dis­tribution of copepods in the upper 500 m ofthe Pacific. Also, at/el/uatus s.l. appears to bea fine particle filter-feeder (Mullin, 1966;Samyshev, 1970) and therefore not a likelycandidate to survive deep submergence to meso-

or bathypelagic depths for periods of one ormore ypars. In the light of this backgroundthe relatively small but constant morphologicaldifferences and an apparent all opatry , main­tained by the formidable barrier of the tropicaland subtropical zones separating the rangesof parki and lal/gae, provide compelling reasonsfor treating the two biantitropical (Brinton,1962) populations as separate species.

If lal/gae could survive transport to temperatewaters of the Northern Hemisphere it could beexpected to appear in the North Atlantic Drift.Despite the great intensity of study on oceaniccopepods of the North Atlantic no "giant"at/el/uatus s.1. forms have been noted from theregion. With (1915, p. 52-53, PI. 1, Figure 6a-c,Text figure lOa-e) reportl-1 l-1everal largeattel/uatus 1-1.1. stage V copepodids (9 = 5.18mm, 0 = 5.0 mm) collected at two North Atlantic10calitiel-1 lying roughly between Iceland andScotland. With notes that "The structure of themouth appendages ... scarcely show differencesof any importance from Giel-1brecht'l-1 del-1cription...". Thul-1 it l-1eems likely that the mandibularbasis in his specimenl-1 bore two setae as insewclli, a l-1pecies that reaches a length in ac­cord with With'l-1 meal-1urements (Figure 16 andl-1ee p. 9!l:~ above). The abl-1ence of other reportsof large atteill/atl/S 1-1.1. in excess of 6 mm in TLfrom the North Atlantic even at considerabledepths (e.g., Roe, 1972) further substantiatesthe lack of a North Atlantic temperate cog­nate ofparki and lal/gae.

The species is named for Bui Thi Lang toacknowledge her discovery (1965) of morpho­logical and geographical complexity in at/ellll­atus s.1.

997

KEY TO THE SPECIES OFEUCALANUS

(Adult Females Only)

Based on integumental organs, all sites aretergal unless specified otherwise.

1. Mxp with four or more pairsof sites; ThIll and IV lackingsingle middorsal site betweenanterolateral hair sensilla;Th IV lacking paired siteslying outside of dorsal quad-rangle of hair sensiIIa 2

Mxp usually with two pairsof sites; ThIll and IV withsingle middorsal site lying be-tween anterior two hair sen-Rilla; ThIV with one pair ofRiteR lateral to quadrangleformed by four hair sensiIIa , 3

2. Mxl and Mx2 with total of 10Rites forming a rectangle andarranged anterior to pORteriorin two bilateral setR of onepair, one single and one pair ofsites; ThII and III in lateralview with three sites, Abd.IV­V with at leaRt three tergalsites attenuatus group, 4

MxI and Mx2 sites vary from8 to 18 in number, not arrang-ed in rectangle pattern. poste-rior sets more lateral thananterior sets; ThII and IIIwith one or two lateral sites;Abd.I-I1 with at least two ter-gal perforations elongatus group, 5

3. ThIll and IV with one medialsite in tergal arc formed by thetergal RiteR. . . .. . .... subtenuis group, 6

ThIll and IV with two medialsites in the arc formed by thetergal sites pileatus group. 7

4. A. Abd.III with tergaJ site " B

Abd.III Jacking tergaJ site " C

998

FISHERY BULLETIN: VOL 71. NO.4

B. Abd.I-lI usually with onesite, Abd.IV-V with threetergal and one pleural site . . . . .. parki

Abd.I-I1 usually with twosites, Abd.IV-V with atleast four tergal and threepleural sites Ian gal'

C. Abd.I-II lacking tergalsites, Abd.IV-V usuallywith five tergal and zeropleural sites selcelli

Abd.I-II with two tergalsites, Abd.IV-V with threetergal, usually two or morepleural sites . . . . . . . . . . . .. attelluatuN

5. A. ThlI and III with a pair ofsites anterolateral to arcformed by tergal sites;Mxl and Mx2 with atleast 16 sites . . . . . . . . . . . . . . . . . . .. B

ThII and III lacking a pairof sites anterolateral toarc formed by tergal sites.Mxl and Mx2 with 12 orfewer sites. . . . . . . . . . . . . . . . . . . . .. D

B. ThI and II each with seventergal sites; Abd.I-II withthree tergal sites , hyalillus

ThI with 13, ThII withnine tergal sites; Abd.I-IIwith four tergal sites . . . . . . . . . . . .. C

C. Mandibular basis with oneseta califorll'icus

Mandibular basis with threesetae . . . . . . . . . . . . . . . . . . . . . " /iu 1/ gii

D. Al somite with sets ofeight and four sites; Mndsomite with six sites; ThVwith three sites; Abd.I-IIwith two sites, Abd.III andIV lacking tergal sites,Abd.IV lacking pleural sites illerl/lis

Al somite with sets of sixand two Rites; Mnd somitewith two to four sites; ThV

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EU(ALANUS

H

B. Mxl somite with t \\" 1':111',;

of sit.es adjal'('I\( t" tlH' Illid·litll'; Abd.l\'-\' wit.h "Ill'site . . . . . .. 81111I'I'(/SS/18

Th I I and I I I with one pairof I' leu ra I si tl'S; Mx~ so­mite lacking tergal sites;AinU-II usually with onesite; Abd.III lacking tergalsites... }lil'<11(/8

6. A.

with four or more sites;Abd.I-II with four or moresites; Abd.I II and IV withtwo or more sites; Abd.IVwith one pleural site. . . . . .. dUlly(//1I8

Mx2 somite with two ormore pairs of sites; ThIwith seven or more sites;Th II and I II with OIH'

asymmetrical site withinarc of hair sensilla on leftof midline; Abd.I-II withtwo sites .

sites;sites

Abd.III with twoB

Mx2 somit" lacking sites;Th I with thrl'l' sitl's; Th I Iand III lacking- sitl'S with·in dorsal :11"(" "f I;;ill" '''''1'11­

la; '\\ll.l-Il I\I! I Ill' ("

one sitl' ('

B. ThI with 1.'5 sites; Mxl so­mite with 10 sites includ­ing a medial set of four; A Isomite with 10 sites includ­ing a posterior set of four;Mnd somite with eight sites 811h/Clllli8

Thl with seven sites; Mxlsomite lacking four medialsites; Al somite lackingfour posterior sites; Mndsomite with four to sixsites , , 1Il1l('/"UI/(//1I8

C. ThII and III with threepleural sites, Abd.IV-Vwith three tergal sites, . . .. II/UI/(/('Ii,IS

ThII and III with twopleural sites, Abd.IV-Vwith one tergal site. . . . . . . . . . . . . .. D

D. Mnd somite with six sites;Abd.I-II lacking tergal sites cm.~,~/{.~

Mnd somite with four sites;Abd.I-II with one tergalsite ,. /ul/g'iccps

7. A. ThII and III with two pairsof pleural sites; Mx2 somitewith two pairs of tergalsites; Abd.I-II with three

Mx 1 ,;"mite with one pair"f ,;itl'S adjacent to t.he mid­line; Abd.IV-V wit.h threesill's tll'II/(///18

USE OF INTEGUMENTAL ORGANSIN STUDIES ON

GEOGRAPHICAL VARIATION

A relatively high degree of \'at'iability inperforat.ion number was noted for the circum­global. broadly tropical spedes, E. slIh/I'l/llis

(Table .1. Figures D, 10). The conspicuousvariability was noticed after realization thatbilateral symmetry and arrangement. in regularpatterns distinguishing species groups as wellas species is characteristic of integument.alorgans. The variation suggested that theseorgans are a promising source to search forevidence of genetic variation in field-collectedplanktonic populations. Thus to carry out apilot study of this possibility the original sam­pling of SlIh/I'llIlis was supplemented by addi­tional specimens sorted at random from zoo­plankton samples selected to represent bothextreme and intermediate geographical loca­tions within the known distribution in eachocean (Figure 20). For each specimen pleuralperforations were tallied from both left andright sides of the entire body and summed withcounts of the tergal perforations to obtain amaximum estimate referred to as the perfora­tion number (PN). TL was also measuredroutinely using procedures described in thesection on Material and Methods. It should benoted that no attempt was made to determinethe existence of geographical variation in any

999

FISHERY BULLETIN: VOL 71. NO.4

20' • '.

O' • ••20' .. •

} 40"

60'

I()()" 100" 60' 20' O'

60"

20"

FIGURE 20.-Geographical distrihution of E/lca/anllll/liJI('IIII;.I. Localities shown hased on records verified hy analysisof integumental organs.

other morphological featureR of subtl'llUis ex­cept to confirm that in virtually all RpecimenRfrom each ocean the mandibular baRiR borethree setae aR found by FukaRe (1957).

The data were first examined by pooling theRampleR from each ocean and comparing themean number of perforations between oceanR.DifferenceR between the pooled Ramples provedto be highly Rignificant (Table 6), and the meanPN values Rhow a pronounced geographicaltrend. The 10weRt mean waR obtained from thePacific Ocean specimenR and the higheRt fromthe Atlantic Ocean specimens. The pooled sam­ple from the Indian Ocean yielded a mean PNvirtually midway between the other two.

The groRR indication of clinal variationRuggeRted further consideration at a finer Rcale.

1000

The PN counts of sulJte/luis were regroupedby geographical source of the Rpecimens in unitRof 60° of longitude and compared in termR offrequency diRtribution and mean PN per geo­graphical Regment (Figure 21). Grouped Ram­pIeR falling within the hydrographic limits ofanyone ocean do not differ significantly (Table7) and Rerve to emphaRize the Rtepped or diR­continuouR pattern of the meanR from the dif­ferent oceanR. The range shown by PN in thetwo geographical RegmentR between long. 30° Eand 150 0 E (Indian Ocean and westernmORtPacific Ocean) Rpans the apparent differenceRin the diRtribution of PN in the Pacific andAtlantic RampleR (Figure 21). ThuR the IndianOcean population would appear to be the onegenetically and geographically intermediate in

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

TABLE 6.-Total number (PN) of perforations in samples of ElIcaJalllls .whlellllis from different oceans.

Sample

Pacific OceanIndian OceanAtlantic Ocean

Range

114-135119-139125-141

123.6388130.0416134.8400

4.97504.99113.2598

2\

24.750624.911110.6263

N

362450

p

Comparison of differences between mean number (Student's 1 - test)

Pacific: IndianIndian: AtlanticAtlantic: Indian-Pacific combined

6074

110

4.8774.989.37

<0.001<0.001<0.001

position to those of the Pacific and Atlanticpopulations, a pattern consistent with the pre­vailing surface circulations of equatorial andwestern boundary currents.

When the various sets of perforations areanalyzed separately, however, the resemblanceof the variation to either a zone of intergrada­tion or a stepped cline disappears. The designat-

ed sites in E. subtel/uis fall into 26 tergal and13 pleural sets based on the scheme describedabove (Figures 5, 7). More than half of thesesets show zero or negligible variability, i.e.,typical perforations were observed at thesesites in virtually all of the specimens. Most ofthe variation was in fact concentrated in onlynine sets of designated sites (Figure 22a, b).

140

til ::::::::::::

C laoo........ass..,£ 125 :;::::s..~

120

9<fw-aoowAtlantic

115

o 2 4 6

1500W-90°(700) WPacific

02460246024602460246

Frequency

FIGlJRE 2t.-Frequency distribution of total number (PN) of perforations per specimen in samples of adult females ofElIcaJallus SUhll'lluis collected within 60° segments of longitude. Uniform large spot shading represents specimens collectedat localities in the Atlantic Ocean; obliquely ruled shading represents specimens collected at localities in the Indian Ocean;irregular finely dotted shading represents specimens collected at localities in the Pacific Ocean. Differences between themeans in the second and third histograms and the fourth and fifth histograms counting from the left are highly signifiicant(I-test, Table 7). Black triangle indicates position of mean PN within geographical segment. All specimens selected at ran­dom from zooplankton samples located in various sectors of the SlIhll'lluis range (Figure 20).

1001

FISHERY BULLETIN: VOL. 71. NO.4

TABLE 7.-Comparison by Studenl's (-test of mean TN values of samples of adulI female .when",;"grouped regionally as in Figure 21 in segments of 60° of longitude.

Regional segments N,+N2 I" P( longitude)

90 0 30oW,30oW·30oE 52 135.74, 134.00 1.99 <0.1 P >0.05300 W _30° E , 30° -90 ° E 45 134.00, 129.56 3.59 <0.00130° ·90oE , 90° -150° E 35 129.56, 128.68 0.54 <0.6 P >0.5900-150 oE,1500 E-1500W 30 128.68, 121.18 5.623 <0.0011500 E-1500W , 150 0 _90° (70 0 )W 23 121.18, 121.25 0.064 >0.9150 0 90 0 (70 0 )W, 9Oo_30 oW 35 121.25 : 135.74 11.91 <0.001

The nine sets appear to vary independentlyof one another, some showing unusually highor low frequencies of absence in one or two ofthe three oceans. In some sets the frequency ofabsence in one ocean differs significantly fromthat elsewhere (Figure 22a, b; Table 8). Withineach set perforations tend to be absent at simi­lar frequencies. Genetic linkage is suggested bythe similar deviations in the Pacific sampleaffecting the following sets: Mxl-T-a-/3, 4, r3, 4;Mxp-T-ll, 2, rl, 2; Thll-P-Ial, ral; ThIll-P­Ial, ral; and ThIV-P-lal, ral.

Also unique to the Pacific sample is the morefrequent occurrence of four perforations on thesomite of the first maxilla (Mxl-T-d-ll, 2, rl, 2).The Indian Ocean sample is distinguished by arelatively infrequent appearance of the set ofperforations on the somite of the second antenna(A2-T-a-/1, 2, rl, 2). The Atlantic sample showsrelatively few absences on the Mxl somite (Mxl­T-c-/l, 2, rl, 2) and on Thll (ThII-T-a-12, 3, r2,3).

In an individual specimen perforations areoften absent in pairs rather than in full setsthough right and left pairs in a set tend to showsimilar frequencies in the sample. Absences ofpeg and pore combinations are usually bilateraland affect both the right and left sides of a parti­cular set. Absences of pairs consisting of a pitsensillum and a pore may be bilateral but morefrequently affect only one side in a specimen.An appreciable portion of the variability in8ulltf'lllli.~ emanates from losses among suchtergal pairs occurring sequentially on the twomaxillary somites. An individual specimen mayshow losses that alternate in successive setsfrom either left to right or the reverse. A notice­able trend in losses toward unbalanced symme­try was found only in the case of Mxl-T-b-ll, 2,

1002

rl, 2. Indian and Atlantic samples showed moreabsences on the right side and Pacific sampleshad a higher frequency of absence on the leftside, but the differences are significant ( X 2 testfor homogeneity) only in the case of the IndianOcean sample (Table 9). Critical examinationfor patterned variation among specimens usinglarger samples may prove to be especialIy usefulfor genetic studies on natural and laboratorypopulations of planktonic copepods.

Despite the relatively frequent absences, eachof the 110 specimens of 8ubtellui8 comprisingthe combined global sample exhibited a re­presentative perforation pattern permittingidentification to species by this feature alone.Also noteworthy is the qualitative resemblancein characters distinguishing the geographicalpopulations of 8ullteuui8 and differences separa­ting parki from langae. As in 8ulltellui8 fewperforations distinguish these alIopatric tem­perate species of the attenuatus group from oneanother, and the sites involved are also restrictedto a limited portion of the body (i.e., the abdo­men and especially Abd.IV-V). The paralIelsemphasize the likelihood of appreciable geneticdiscontinuity separating Atlantic, Indian, andPacific populations of .~/llIt(·llui8 that deservesmore intensive study.

SIZE AND PERFORATION NUMBER

The perforation number (PN), i.e., the num­ber of designated sites in the species observedon each specimen is derived from a meristiccomplex of integumental organs. The two organsystems, sensilla and glandular pores, arearranged in serially homologous sets that aredistributed on all body segments. Showingphylogenetic and species specific patterns, they

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

A

~·· ....:.~ •.. ··9

.. 3'...

~

fd75 C

a c

FIGURE n.-Variation in the occurrenceof perforations at designated sites in threeregionally pooled samples of El/ca/a/ll/s

sl/ble/ll/is adult females. Sampling locali­ties shown in Figure 20 and geographicalgrouping based on significant differencesbetween geographical regions shown inTable 7. From the left: Atlantic Oceansample (N = 'iOl. Indian O"ean sample(N = 24). Pacific Ocean sample (N =36). Dots represent perforation sitestypical of the species. Numbers representpercentage of specimens lacking a per­foration at this site; open circles enclosepairs of sites showing the same frequencyof absence. Absence of a number indicatesperforation found in all specimens ofthe sample. Dorsal view top: rightlateral view bottom.

1008

FISHERY BULLETIN: VOL. 71. NO.4

TABLE g.-X2 test for homogeneity of frequency of ahsence of perforations from designated sites among geographicallydifferent samples of ElIcu/w/lIs slIhteflllis adult females described in Figures 20 and 21.

Regional sampleN

Designated sites(no.)

Frequency of absences

Atl. Ind. Pac.50 24 36

Atl., Ind., Pac.comnared

X2 P2d.f.

Atl., Ind.compared

X2 Pld.f.

Atl., Pac.compared

X2 Pld.f.

Ind., Pac.compared

X2 Pld.f.

largestsourceof X2

A2·Ta2:11,2;rl,2

(4 sites)

Mxl·Ta2:/3,4;r3,4

(4 sites)

Mxl·Tc2:11,2;rl,2

(4 sites)

Mxl·Td2:/1,2;rl,2

(4 sites)

Mxp·T~/I,2;rl,2

(4 sites)

Thll·Ta~12,3;r2,3

(4 sites)

Thll.Pr,1~al

(2 sites)

Thlll·PrJ~al

(2 sites)

15

29

75

168

59

14

4

4

55

4

62

94

34

58

6

6

23 99.8 <0.001 89.2 <0.001 5.28 <0.025P>O.Ol

106 179.9 <0.001 6.98 <0.01 122.2 <0.001P>0.005

88 27.5 <0.001 19.1 <0.001 18.7 <0.001

96 39.3 <0.001 12.3 <0.001 14.1 <0.001

100 57.7 <0.001 1.0 <0.5 53.8 <0.001P>0.25

98 156.2 <0.001 100.7 <0.001 142 <0.001

28 32.3 <0.001 -0.8 <0.5 22.2 <0.001P>0.25

28 33.3 <0.001 3.7 <0.1 30.2 <0.001P>0.05

44.6 <0.001 Indian

108.2 <0.001 Pacifoc

0.26 <0.75 AtlanticP>0.5

29.1 <0.001 Atlantic

27.1 <0.001 Pacifoc

1.48 <0.25 AtlanticP>O.1

18.0 <0.001 Pacifoc

8.3 <0.005 PacifocP>O.OOl

ThIV·Pr,12: 01

(2 sites)

No. X 2 with P '% 0.5

2 17 26.0 <0.001

9

o >0.9

5

18.7 <0.001

9

9.5 <0.005P>O.OOI

7

Pacific

are the unmistakable phenetic expression of thegenotype.

Body size (TL) is a priori also under geneticcontrol, and probably in copepods this controlis rigorous (Brooks and Dodson, 1965; Brooks,1968; Dodson, 1970; June and Carlson, 1971).However, it is known that in addition to selec­tion pressures diet and temperature may strong­ly influence size determination (Coker, 1933;Deevey, 1960, 1964, 1966; Omori, 1970). Aquestion of immediate concern is whether TLand PN may be sufficiently related to showsimilar phenetic patterns of variation.

Morphogenesis during the copepodite phaseof ontogeny appears to affect PN in a simplepredictable fashion. In general, copepodid stages

1004

III, IV, and V were found with the same num­ber and arrangement of sites, segment by seg­ment, as they appear in adults of the specieswith exceptions in abdominal segments asindicated above. The exceptions noted arerestricted to ontogenetic modifications in theaddition of abdominal segments and subsequentfusion of segments brought on by sexual matu­ration. Thus at least during the second half ofontogenesis integumental organs maintainnumerical and distributional relationshipsduring typical size increases associated withmoulting; no observations are available forcopepodite stages I and 11. If a relationshipexists between TL and PN it should be apparentfrom comparison of the two within a given onto-

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

T ABLE 'I.-Frequency of absence of perforations at adesignated site in EI/Ca/lIIllls SI/hlelll/is ('7r).

TABLE JO.-Correlation coefficient (r) of TL and PN inadult females of Ellca/alll/s. Original measurements showngraphically in Figures 10. 12. 14. 16.

genetic stage. In making such comparisons,however, it should be recalled that considerationslimited to the numerical value of PN is mean­ingful primarily within a species group. Be­tween groups numerical differences in desig­nated sites may not occur, but the speciesalways differ in topographic arrangement ofsets of perforations common to their respectivegroup (Figures 9,11,13,15).

Scatter diagrams of TL and PN (Figures10, 12, 14, 16) show no common pattern of re­lationship among the 19 distinguishable popu­lations (i.e., including the three geographicalpopulations of subtelluis). Pearson's product­moment correlation coefficients were calculatedfor the available measurements of each popula­tion (Table 10). Eleven were positive correla­tions and eight were negative, a division in­dicative of the absence of a real relationshipbetween TL and PN in the genus. Only four ofthe correlations depart significantly from zero(5% level): three are positive correlations andone is negative. All aspects considered, the foursignificant correlations, i.e" SIl!Jtl'llIlis, PacificOcean (+), 1I1I1('/,II/lOtIlS (+), sl'l/'l'lli (+), and1II1I/IUChus (-) are probably spurious. Thus,as a working hypothesis PN and TL may beconsidered to vary independently in adultfemale EII('alrwus.

These data shed light on another vital questioninvolving TL and PN, namely, whether in factthe two characters are related genetically. Wemay anticipate that such a relationship wouldbe apparent by the correlation of the two charac­ters in each species group.

Figures 10, 12, 14, and 16 in fact clearlyshow the absence of uniformity in the relation­ship of TL and PN across the genus. We findthat each group presents a different pattern ofrelationship between TL and PN.

left 1. 2 right 1, 2 X2, ld.l.

Designated site:

Mxl-T-6

Sample

Pacific OceanIndian OceanAtlantic Ocean

28, 2817, 1720, 20

19,19 -1.637, 37 5.2832, 32 3.64

P

<0.25 P>0.2<0.025 P>0.02<0.1 P>0.05

Species N P

\'llhlt"'lli.\':

Atlantic 50 0.0241 >0.1Indion 24 .1683 >0.1Pacific 36 .3586 <0.05 P >0.02

mucronaul\ 20 .4743 <0.05 P >0.02crcnslIs 10 .3477 >0.1!lHlRin'/H 12 -.3311 >0.1mlJlul('hlts 17 .5967 <0.02 P >0.01pileat".\ 20 --.3556 >0.1\lIhcrassH.\ 34 .1569 >0.1dentalll\ 21 -- .0543 >0.1e!on1-:atIH 19 -.0518 >0.1l1.\'al/11I1\ 25 .0831 >0.1j11ermis 16 .2365 >0.1"/lIlRi; 15 .0434 >0.1cllJi./inniClH 22 .3241 >0.1artentiCltlH 26 .0498 >0.1, ('welli 43 .3446 <0.05 P >0.02parki 17 .0407 >0.1laIlRCl(' 14 .0565 >0.1

It would be of considerable interest to knowif PN relates to geographical overlap in thebreeding range of species of the same speciesgroup. Another related question of ecologicalsignificance is whether TL varies with the ex­tent to which the range of a species falls outsideof the ecological or biogeographic regionstypically occupied by the species group.

REMARKS ON THE FUNCTION OFINTEGUMENTAL ORGANS IN

EUCALANUS

With so few available retinal cells (Vaissiere,1\)61; Fahrenbach, 1962, 1964; Park, 1966),copepods must locate appropriate sexual part­ners, couple, and accomplish spermatophoretransfer and attachment in the apparent ab­sence of visual contact with the environment. Innature the available methods appear to beeminently successful in preventing hybrid pair­ing and in ensuring functional placement of thespermatophore's discharge canal on the femalegenital pore (Fleminger, 1967; Frost and Flem­inger, 1968). External chemical and mechanicalreceptor-effector systems among the CruRtaceaappear sufficiently diverse to provide adequatenon-visual channels mediating the exchange ofinformation required by a relatively complex andefficient, inRtinctive mating behavior. AR in

1005

terrestrial arthropods microanatomical studieson copepods (Lowe, 19,35; Fahrenbach, 1D62;Park, 1966) reveal a highly organized centralnervous system, one that supports inner­vated integumental sensilla and glands distri­buted symmetrically over the body. Thereceptors may monitor the environment, andthe effectors may release information in responseto appropriate stimulators.

Among semispecies, i.e., somewhat differen­tiated populations ofa superspecies (Mayr, 1970),the primary reproductive barrier is extrinsicinasmuch as potential hybridizers lack accessto one another. Assuming no significant contactsince the inception of allopatry, intrinsic repro­ductive barriers, Le., prezygotic mechanisms, ifany, are untested and probably imperfect ornonexistent. Similar populations of recentcommon ancestry newly brought togetherthrough the expansion of ranges are likely tointeract unfavorably across a spectrum of fun­damental organismic processes and thereby ex­perience pronounced selection pressures. Whensympatry replaces allopatry among sets ofsemispecies hybridization is often intense in thearea of geographical overlap (Remington,1968; Rising, 1970).

The only stabilizing alternatives for suchinteracting populations are: 1) elimination ofone or both; 2) genetic displacement; or :3)coalescence. Alternatives 1 and 2 will prevailif, in general, hybrid offspring are less fit and ata selective disadvantage and only postzygoticbarriers are available. Development of increasedefficiency of prezygotic barriers will be at apremium and the rate of their development anddistribution will be a function of the rate ofinteractions and the mobility of the populations.According to MacArthur and Wilson (1967) acomputer model by Bossert has indicated thatfull displacement is achieved rapidly and, underideal conditions, equilibrium may be achievedin as few as 10 generations.

As seen in each of the species groups of EI/(,o­101/us, differences in the integumental organsbetween species groups include features com­mon to all members and those common to mem­bers comprising the group. Within a groupdifferences tend to occur on or near the genitalsegment. Moreover, there is a general trend for

1006

FISHERY BULLETIN: VOL. 71. NO.4

differences to be more pronounced in the popula­tions whose distributions are most extensiveand bring them into contact with the largestnumber of other members within the speciesgroup. Thus, the pattern of integumental organsin Eu('olouus show configurations that appearto have been shaped by character displacement(Brown and Wilson, 1956) in the broadest senseor what some (Blair, 1963; Littlejohn, 1965)have referred to as reinforcement. If so, inte­gumental organs in copepods may play asignificant role in the mating process.

CONCLUSIONS

1. This study provides unique and compellingevidence of the extensive information contentapplicable to systematics, phylogenetics, evolu­tion, and population biology present in the in­tegumental sensor.'! and effector organs ofplanktonic copepods.

2. Integumental organs appearing on thebody segments in Euco[ouus are distributed inbilaterally symmetrical, serially homologouspatterns that appear in both dorsal (tergal) andlateral (pleural) sets corresponding to the so­mites of the body. The organs fall into two basicgroups: a) receptors that appear as hairs, pegs,or pits and b) integumental glands that commu­nicate with pores on the surface of the exoskele­ton. Within the set of a somite each designatedsite is constant in position and in morphologicaltype of organ relative to the others comprisingthe set.

:3. Analysis and survey of the gross morphol­ogy, distribution, and variation of these integu­mental organs was facilitated by a combinationof techniques including a) digestion of internaltissues and intensive staining for light micros­copy, b) clearing and integumental staining ofintact specimens for light microscopy, and c)scanning electron microscopy. Processing ofrelatively large numbers of specimens wasaccomplished most efficiently using method a.

4. Comparative survey ofintegumental organsin 17 species recognized in this study as com­prising the genus Eucalallu.~ indicated that thenumbers and arrangement of these structuresreflect generic similarities, species group simi­larities, and individual species patterns, all

FLEMINGER: INTEGUMENTAL ORGANS IN GENUS EUCALANUS

species but one pair being sufficiently distinctivein number and arrangement to be identifiable .solely on the basis of integumental organs.Species grouped on the basis of integumentalorgans concur with groupings that utilize theseminal receptacle. segmentation of the abdo­men and structure of the male fifth legs. Ingeneral, variation was negligible; about 80% ofthe sites in each species was observed in allspecimens examined and an additional 10% ap­peared in from 80 to 99% of the specimens. Themean number of organs observed in samplesof each population ranged from a low of 83 to ahigh of 135 in a combined total of 448 randomlyselected specimens representing the 17 speciesin the genus.

5. Comparison of geographical relationshipsand number of integumental organs withineach species group indicates that the specieswith the broadest geographical range is also theone with the most distinctive number or ar­rangement of integumental organs especial­ly with respect to organs on the genital seg­ment. The combination of species specificity,phylogenetic relationships, and geographicalpatterns associated with numbers and ar­rangement of organs indicate that the organsmay function in prezygotic mating barrierswithin thp. genus.

6. Comparison of total length and number ofintegumental organs indicates that the twofeature,~ are unrelated.

7. Variation in integumental organs in thecircumglobal broadly tropical species E. slib/c­

illl i.~ was found to have a strong geographicalpattern indicating limited gene flow betweenthe populations of the Eastern Tropical Pacific,the Indo-West Pacific, and the Atlantic Ocean.Some sets of organs were found to vary inde­pendently; others appeared to vary similarlyproviding evidence that the genetic control iscomplex. Their responses to selection pressuresappear to vary sufficiently to warrant detailedstudy of .~ub/cllllis in relation to its closestcognate, IIII/crolio/lls, within and outside oftheir reg'ion of co-occurrence.

8. Limited examination of males and cope­podid stages III to V indicate that the integu­mental organs appear in the same numbers andarrangements that characterize the adult female

except for structures that have not yet com­pleted sexual maturation or are sexually dimor­phic.

9. The attenuatus complex is revised on thebasis of integumental organs and geographicaldistribution. Four biologically discrete popula­tions are recognized, three being described asnew species.

ACKNOWLEDGMENTS

This research was supported by NationalScience Foundation Grants (GB 12412, GA31092, GB 32076) and by the Marine Life Re­search Group of Scripps Institution of Oceano­graphy. I am particularly grateful to my twocolleagues: K. Hulsemann whose meticulousediting and compilation of the manuscriptsignificantly improved its accuracy and expe­dited its completion and J. Behrhorst who car­ried out scanning electron microscopy and pre­pared Figure 2.

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