Hydrobiologia 292/293 : 341-349, 1994 .F D. Ferrari & B. P Bradley (eds), Ecology and Morphology of Copepods.©1994. Kluwer Academic Publishers. Printed in Belgium

Latitudinal diversity patterns of continental benthic copepod speciesassemblages in the Americas

J. W. ReidDepartment of Invertebrate Zoology, NHB-163, National Museum of Natural History, Smithsonian Institution,Washington, DC 20560, USA

Key words : Copepoda, Cyclopidae, Harpacticoida, latitudinal distribution, Americas, biodiversity, conservation

Abstract

The diversity, considered as richness (numbers) of genera and species, of continental benthic Copepoda of theAmericas was examined. Thirty-three local lists of planktonic and benthic Cyclopidae (Eucyclopinae and Cyclop-inae), 21 local lists of epibenthic Harpacticoida (Canthocamptidae), and 8 local lists of interstitial Harpacticoida(Parastenocarididae) were compared . Available data do not allow the rejection of the null hypothesis of no signifi-cant difference in diversity of tropical and temperate copepod faunas . For Cyclopidae, 6-15 genera and 6-44 specieswere recorded from local areas ; linear regression analysis showed no significant correlation between latitude andnumber of genera and species . For Canthocamptidae, 1-13 genera and 3-43 species were recorded locally, withno significant correlation between latitude and number of species ; for genera the correlation between latitude andnumber of genera was strongly positive, but the effect of latitude is small . No relationship between latitude anddiversity of the Parastenocarididae was evident from inspection . Endemism of Cyclopidae and Canthocamptidae issignificantly greater in South America, as shown by comparisons of Sorensen's similarity coefficient between pairedareas. Because of this high degree of endemism, conservation strategies for South American wetland invertebratesshould emphasize preservation of many small sites .

341

Introduction

Global or regional latitudinal patterns of diversityhave been analyzed for many groups of terrestrial,marine and continental (freshwater) arthropods andother invertebrates . In several cases the diversity pat-terns that might be expected from analogy with ter-restrial vertebrates, that is markedly higher speciesrichness in tropical regions, are not evident. Forinstance, some groups of spiders are most speciose incool temperate climates (Platnick, 1991), and marineamphipods have at least as many known species at thepoles as in the tropics (Barnard, 1991) . For estuar-ine planktonic copepods of eastern North America, thehighest cyclopoid species richness occurs in the sub-tropics, but calanoid species richness is highest in thetemperate zone (Turner, 1981) . Patalas (1990) foundthat the diversity of zooplankton communities in Cana-dian lakes is highest at mid-latitudes, where north-ern and southern species coexist . Freshwater calanoid

copepods in Brazil are distributed in a similar pattern(Matsumura-Tundisi, 1986) . The poverty of the trop-ical freshwater plankton including copepods is gener-ally accepted as a real phenomenon (Lehman, 1988),although the reasons for this difference are unclear(Dodson, 1992) . In some contrast to the results ofPatalas (1990), Dodson (1992) found no significantrelationship between species richness and latitude ofzooplankton in 66 North American lakes, but ratherlake size, average rate of photosynthesis and numberof neighboring lakes within 20 km accounted for mostvariation. Similarly, in European lakes, the speciesrichness of crustacean zooplankton was positively cor-related with lake area, but not with latitude or longitude(Dodson, 1991) . On the other hand HernAndez-Trujillo(1991) demonstrated higher copepod species richnessin southern, warmer waters off Baja California Sur,Mexico .

Studies of American copepods are well into theirsecond century and provide an extensive body of data

342

on the composition of local faunas . Certainly the num-ber of known species continues to rise, rapidly in recentyears because of increasing interest in non-lacustrinewetlands (Reid, 1992), and because of the growth ofthe limnological sciences in many countries . Althoughthe copepod fauna of the Americas is still little knownrelative to that in Europe (Reid, 1992), collectors havevisited most types of surface lakes, rivers and wetlandsfrom the Arctic to Tierra del Fuego, often samplingthrough one or more annual cycles . If there exists abias in this database, it is in favor of tropical areaswhich have attracted a good deal of attention in recentdecades .

This article compares patterns of latitudinal diver-sity, considered simply as richness (numbers) of generaand species, of the three dominant groups of benthiccontinental Copepoda: the Cyclopidae (Eucyclopinaeand Cyclopinae) and the harpacticoid families Cantho-camptidae and Parastenocarididae .

Methods

The total number of species and genera of planktonicand benthic continental Cyclopidae known from eachof 33 local areas was compared . The lists were restrict-ed to Eucyclopinae and Cyclopinae, excluding the fewspecies of the euryhaline-coastal Apocyclops . 'Plank-tonic' cyclopids were included because for these ani-mals the distinction between `plankton' and 'benthos'is often meaningless . Twenty-one local lists of epiben-thic Harpacticoida (Canthocamptidae) and 8 local listsof interstitial Harpacticoida (Parastenocarididae) werecompared .

Species lists were generated from compendia suchas Dussart & Defaye (1985, 1990) and Reid (1985,1990), additional recent publications, articles in press(e.g . Chengalath & Shih, 1993; Reid, 1994a, 1994b ;Reid & Marten, 1994), and from unpublished data (e.g .Adams et al., 1992 ; Ebert, 1976; Reid, unpublished) .Lists of the particular areas considered and the speciesincluded for each are available from the author .

The species lists were organized by country, majorarea, state or province . Areas were selected for analy-sis according to the general criteria that they have beenvisited by experienced collectors, at least some habitatsin addition to lakes and ponds were investigated, andthe taxonomic work is relatively recent. Species listswere included from both vast (e.g. Argentina northand south of 50 °S ; Brazilian Amazonia) and rela-tively small areas (e.g. the State of North Carolina,

USA). However, general knowledge of the fauna maybe equivalent depending on the history of limnologicalinvestigations in the area. These imbalances should beborne in mind by the reader, but tend to even out overthe large scale considered.

The latitude assigned was usually the geographicalcenter of each area, moved in a few cases to the cen-ter of most collecting activity. For areas at identicallatitude, the latitudes assigned differ by one degree .

Two aspects of the species lists were considered .First, the relationship of the total numbers of gen-era and species in each area to latitude was examinedgraphically (Figs. 1, 2) and analyzed by simple linearregression (Table 1) for the Cyclopidae and the Can-thocamptidae . Because the Parastenocarididae are rel-atively poorly known, numbers of genera and species(Table 2) were compared by inspection .

Second, the values of St rensen's similarity coeffi-cient between paired areas were calculated and mappedfor the Cyclopidae and the Canthocamptidae (Figs . 3,4). Canthocamptidae in Ecuador are poorly known anddata for that country, although similarity coefficientsare mapped in Fig . 4, were not included in calculations .

Results

In temperate North America there are about 95 knowncyclopid species in 16 genera ; 108 species in 22 generaoccur in the tropics . Some 46 species in 12 genera areknown from Argentina, Chile and Uruguay together .The number of genera recorded from a particular regionvaries from 6-15 and the number of species from 6-44(Fig. 1) . The regression of both number of genera andnumber of species on latitude is slightly negative, withnon-significant values of r (Table 1) .

In temperate North America there are about 62known species in 12 genus-groups of Canthocamp-tidae, vs about 70 species in 9 genus-groups in theneotropics . In Argentina, Chile and Uruguay togetherthere are 63 species in 8 genus-groups . The numberof genera per area varies from 1-13 and the numberof species from 3-43 (Fig . 2). There is a strong posi-tive correlation between number of genera and latitude,although the effect of change in latitude on number ofgenera is small (Table 1) . There is no significant rela-tionship between number of species and latitude .

In the case of the Parastenocarididae, most collect-ing effort has been expended in Brazil and Argentinaand only the species lists from those areas are suit-able for comparison, although lists from eight areas

50

40

30

20

10

Number ofGenera

CyclopidaeLatitudinal Diversity

65P635554524544423936353027262219181510 8 6 5 0 1 8 1216242633344452S

Degree of Latitude

Number ofSpecies

Fig. 1 . Numbers of genera and species of the Subfamilies Eucyclopinae and Cyclopinae (Cyclopidae, Cyclopoida) recorded from 33 areas inthe Americas, from 65 ° north latitude (extreme left of abscissa) to 52 ° south latitude (extreme right) .

Table 1 . Equations for linear regression of number of genera and species (y) on latitude(x), r values, and coefficients of variation (CV) of American continental Cyclopidaeand Canthocamptidae. NS indicates not statistically significant (p>0.05) ; ** indicatessignificant at 99% level (p<0 .01).

are shown in Table 2. The numbers of taxa now knownfrom the Amazonian and central highlands (cerrado)regions of Brazil are slightly lower than the numbersknown from northern Argentina .

Comparison of the species composition of pairedcopepod communities reveals that in North Ameri-ca, these communities tend to be composed of sim-ilar species over broad regions (Figs . 3, 4) . However

343

in South America, the species composition changesradically within relatively short distances. Both thecyclopids, which are better known and include a rel-atively high proportion of broadly distributed species,and the less well-collected, more highly endemic can-thocamptids follow this pattern .

Comparing cyclopoid communities north of Mex-ico, the mean value of Sorensen's similarity coeffi-

Taxa Regression equation r CV (%)

Cyclopidae (genera) y = -0 .00336x + 10 .7344 0 .025 (NS) 22 .7Cyclopidae (species) y = -0 .04343x + 23 .6600 0.092 (NS) 38 .3Canthocamptidae (genera) y = 0 .08217x + 3.1174 0.583 ** 48 .9Canthocamptidae (species) y = 0 .14285x + 10.7960 0.314 (NS) 59 .2

344

50

40

30

20

10

0

CanthocamptidaeLatitudinal Diversity

65N 61 55 54 52

Number ofGenera

46 42

Table 2 . Numbers of genera and species (species in parentheses) ofAmerican continental Parastenocarididae (Harpacticoida) by regionand latitude.

Primary references : °Dussart & Defaye (1990) ; (b)Reid (1990) ;°Reid (1991) ; dReid (1994a, 1994b) ;'Strayer [1988 (1989)1 ;f Reid (unpublished).

cient (SSC) between 23 pairs of areas was 0 .59 (range

39 36 22 18 8 7 5Degree of Latitude

0 12

Number ofSpecies

16 24 34 40 52S

Fig. 2 . Numbers of genera and species of the Family Canthocamptidae (Harpacticoida) recorded from 21 areas in the Americas, from 65°north latitude (extreme left of abscissa) to 52° south latitude (extreme right) .

0.38-0 .80) . For cyclopoid communities in 17 pairs ofareas in northern continental South America (exclud-ing Uruguay, Argentina and Chile), the mean SSC was0.32 (range 0.13-0.46). These means are significantlydifferent (t = 8.071, p < 0.01) . The cyclopoid com-munities of Chile, northern Argentina, and Tierra delFuego are not especially closely related, having SSCvalues from 0.16-0.40 (mean 0.31, n = 3) . This ispartly because the cyclopoid community of northernArgentina is a transition zone with a large proportionof tropical species .

For 16 paired canthocamptid communities northof Mexico, the mean value of SSC was 0 .49 (range= 0.17-0 .86). For canthocamptid communities in 12paired areas in northern continental South America, themean SSC was 0.10 (range 0-0 .28). These means aresignificantly different (t = 4 .96, p < 0 .01). The cantho-camptid communities of Chile and Argentina are bothspecies-rich and highly endemic (mean SSC = 0.09,range 0.04-0.15, n = 3) . As with the cyclopoids, there

Region ° Lat . Genera (species)

New York State' 42N 1 (3)Honduras° , b 15N 1 (2)El Salvador° , b 13N 1 (6)Venezuela° 8N 1 (1)Brazilian Amazonia°'f 0 2 (16)Brazilian Highlandsd 16S 3 (19)Sao Paulo State, Brazil °, ° 24S 3 (10)Argentina (north of 50 I S)' , c 34S 3 (21)

345

Fig. 3. Values of Sorensen's index of similarity between 33 paired regional species lists of Eucyclopinae and Cyclopinae (Cyclopidae,Cyclopoida) .

346

Fig. 4. Values of Sorensen's index of similarity between 22 paired regional species lists of Canthocamptidae (Harpacticoida) .

is a slightly greater degree of similarity between thecanthocamptid species lists from northern Argentinaand the neotropical lowlands .

There are no species of the Parastenocarididae incommon between the areas listed in Table 1 .

Discussion

Tropical and temperate continental copepods are close-ly related, with only three families, the cyclopoidCyclopidae and the harpacticoid Canthocamptidae andParastenocarididae, dominating the world freshwaterbenthic faunas . Several genera occur throughout mostof the Americas (Attheyella s . I ., Epactophanes, Eucy-clops, Homocyclops, Mesocyclops, Microcyclops,Paracyclops, Parastenocaris, Tropocyclops) . There islittle indication in the data presented here of a correla-tion between latitude and species or genus richness byarea for the three groups considered . That is, the totalnumber of species and genera present in a particulargeographical area is approximately the same . Confa-milial and congeneric species probably play broadlysimilar, although not identical, roles in their respec-tive ecosystems . Similarly structured systems may beassumed to support a similar number of species . There-fore, the approximate equivalency in total numbers ofbenthic copepod species occurring in both temperateand tropical local areas appears to indicate that thehabitat structures of tropical and temperate-zone ben-thic aquatic environments do not differ much, at leastas regards the copepods ; that is, both tropical and tem-perate areas afford a similar number of niches .

The only statistically significant relationshipbetween diversity and latitude found here is the weakpositive correlation between latitude and the numberof canthocamptid genera . This results from the well-established fact that certain genera are more successfulin tropical than in temperate zones, and vice versa .For example, the canthocamptid genus Elaphoidel-la is most speciose in the tropics, with 17 speciesdescribed from Cuba (Reid, 1990), but only 9 speciesknown from North America north of Mexico (Reid& Ishida, 1993) . Several canthocamptid genus-groupsdominate in cool climates, e .g . Delachauxiella in theAndes and temperate South America, and Attheyellas . str. and Mrazekiella in temperate North America .Canthocamptids in general are most successful in coolhumid climates worldwide, and in the Americas attainthe highest known diversities in southeastern Alaska(Wilson & Yeatman, 1959), Patagonia and the Andes

347

(Dussart & Defaye, 1990) . Twenty-four species of can-thocamptids were collected by Reid (1993a, 1993b)from the tropical but relatively arid central Brazil-ian highlands . By comparison, Lewis (1984) listed 35species of canthocamptids in cool humid New Zealand .Hamond (1987) reported 26 species in Australia, mostfrom the southern and eastern part of the continent andfrom Tasmania . The latitudinal replacement pattern ofcanthocamptid genera suggests that there are no com-peting `ecological analogues' from other invertebrategroups which might account for lower tropical diver-sity, contrary to the argument of Stevens (1989) .

Several factors appear to contribute to species rich-ness of local communities of continental cyclopoids .Areas of overlap between faunas characteristic of dif-ferent areas are highly speciose. One such area in SouthAmerica is northern Argentina, where tropical and tem-perate species coexist (Reid, 1985) . In Canada, Patalas(1990) found the greatest number of planktonic speciesin the center of the continent where the ranges of manynorthern and southern species overlap . Some areas mayafford a wide variety of niches within a relatively smalldistance, such as Venezuela, which has a large numberof cyclopid species (42, including 6 endemics) . How-ever, the degree of faunal endemicity of cyclopoidsis much lower than in harpacticoids and there are noknown particularly speciose centers of endemism ofcyclopoids .

The most extreme endemism at species level occursin the Parastenocarididae . There is no species in com-mon between the best-investigated locales in SouthAmerica (Table 2) . The limited known ranges of mostspecies in this family can be ascribed to lack of vagilityof these exclusively interstitial animals. On the otherhand, species-groups and genera occur over a conti-nental or multicontinental scale, according to presentlylimited systematic understanding .

There is no great difference between the totalnumbers of species and genera of Parastenocarididaeknown from tropical Amazonia, and the numbers frommore temperate northern Argentina. This family is theleast investigated of the three considered here, andsome of the areal differences must be ascribed simplyto historical differences in collecting effort . However,at least as much effort has been expended in Amazo-nia as in northern Argentina, and the high number ofspecies now recorded from temperate Argentina mayreflect equivalent faunal richness in both areas .

Platnick (1991) pointed out that it is fallacious toassume that patterns of animal distribution will be sim-ilar in the northern and southern temperate zones . His

348

contention is borne out by the high degree of endemismin both the cyclopoid and canthocamptid communi-ties of southern South America, versus the much low-er degree of endemism observed in temperate NorthAmerica. Rapoport's rule that tropical species tendto have narrower latitudinal ranges than temperatespecies (Rapoport, 1982) appears to hold for NorthAmerican, but not for South American temperate ben-thic copepods .

The nature of continental copepod distribution pat-terns has implications for wetlands conservation . Plat-nick (1991) advised that conservation planning takeinto account questions of the degree of endemismof local faunas, noting that areas of high endemismexist in the temperate zones as well as in the trop-ics. Certainly the canthocamptid faunas of southernChile and Argentina and in the Andes uplands areboth diverse and highly endemic, rivaling or exceedingspecies numbers present in the neotropical lowlands .Endemism for both canthocamptids and cyclopids ismuch greater in all of South America than in temper-ate North America . If the distribution patterns of otheraquatic invertebrates are similar to those of copepods,in the tropics and temperate South America it will beimportant to preserve a large series of wetland sites,even though individual sites may be small and the habi-tats may seem similar. If only a few examples of dis-similar wetland habitats are preserved, many specieswith restricted geographical ranges will be lost .

Both Barnard (1991) and Platnick (1991) indicat-ed that the view of animal distribution gained fromthe study of invertebrates is quite different from theviewpoint of vertebrate zoologists . The assumption ofhigh tropical biodiversity is not valid for all inverte-brate groups, and the American continental benthiccopepods provide a good example .

Acknowledgements

I am grateful to Dr Chang-tai Shih for his permission toinclude data from a prepublication copy of Chengalath& Shih (1993). Mr William F. Adams kindly autho-rized use of data in the unpublished report by Adamset al. (1992) . Several colleagues, notably Drs GeraldG. Marten and Marco F. Suarez, collected the materi-al on which many unpublished records are based . DrsThomas E . Bowman, Stanley I . Dodson, Frank D . Fer-rari and David L . Strayer commented helpfully on themanuscript . Drs C. Herbert Fernando and Edward B .Reed suggested additional references .

References

Adams, W. F. (compiler), J . M . Alderman, D . J . DeMont, J. W. Reid,A. Y Taylor & D. J. Williams, 1992. A report on the conservationstatus of North Carolina's Freshwater and Terrestrial CrustaceanFauna. Scientific Council on Freshwater and Terrestrial Crus-tacea . Unpublished report to North Carolina Wildlife ResourcesCommission. Raleigh, North Carolina, 77 pp .

Barnard, J. L., 1991 . Amphipodological agreement with Platnick . J.nat. Hist ., Lond . 25 : 1675-1676 .

Chengalath, R . & C .-t . Shih, 1993 . Littoral freshwater copepods ofnorthwestern North America : Northern British Columbia. Verh.int . Ver. Limnol . In press .

Dodson, S., 1991 . Species richness of crustacean zooplankton inEuropean lakes of different sizes . Verh . int . Ver. Limnol . 24 :1223-1229 .

Dodson, S ., 1992 . Predicting crustacean zooplankton species rich-ness . Limnol. Oceanogr. 37: 848-856.

Dussart, B . & D . Defaye, 1985 . Repertoire mondial des CopepodesCyclopoIdes . Editions C .N.R.S ., Bordeaux, 236 pp .

Dussart, B. & D. Defaye, 1990. Repertoire mondial des crustacdscopdpodes des eaux intdrieures . III . Harpacticoides . Crustaceana,Suppl. 16 : 1-384 .

Ebert, S ., 1976. NatUrliches System and Biogeographie der Fam-ilie Canthocamptidae (Copepoda Harpacticoida) am Beispielneotropischer Taxa . Ph . D . Dissertation, Christian-Albrechts-Univ., Kiel, 335 pp .

Hamond, R., 1987. Non-marine harpacticoid copepods of Australia .I. Canthocamptidae of the genus Canthocamptus Westwood s .lat . and Fibulacamptus, gen . nov ., and including the descriptionof a related new species of Canthocamptus from New Caledonia.Invert . Taxon . 1 : 1023-1247 .

Herndndez-Trujillo, S . 1991 . Variaci6n latitudinal de la diversidad decopepodos en In costa occidental de B . C . S ., Mexico 1982-1984 .Cienc . mar. 17 : 83-103 .

Lehman, J . T., 1988 . Ecological principles affecting communitystructure and secondary production by zooplankton in marineand freshwater environments . Limnol . Oceanogr. 33 : 931-945 .

Lewis, M . H ., 1984. The freshwater Harpacticoida of New Zealand :a zoogeographical discussion . Crustaceana, Suppl . 7, Stud . Cope-poda . 2 : 305-314 .

Matsumura-Tundisi, T. 1986 . Latitudinal distribution of Calanoidacopepods in freshwater aquatic systems of Brazil . Rev . brasil .Biol . 46 : 527-553 . (Includes errata sheet for p. 551) .

Patalas, K ., 1990. Diversity of the zooplankton communities inCanadian lakes as a function of climate . Verh. int. Ver. Limnol .24:360-368 .

Platnick, N . I., 1991 . Patterns of biodiversity: tropical vs . temperate.J . nat . Hist., Lond . 25 : 1083-1088 .

Rapoport, E. H. 1982 . Areography: geographical strategies ofspecies . Pergamon Press, Oxford, 269 pp .

Reid, J . W., 1985 . Chave de identificaclio e lista de referdnciasbibliogrhficas para as espdcies continentais sulamericanas de vidalivre da ordem Cyclopoida (Crustacea, Copepoda) . Bolm Zool .,S . Paulo 9 : 17-143 .

Reid, J . W., 1990. Continental and coastal free-living Copepo-da (Crustacea) of Mexico, Central America and the Caribbeanregion . In : D . Navarro L . & J . G . Robinson (eds), DiversidadBiblogica en la Reserva de la Biosfera de Sian Ka'an, Quin-tana Roo, Mexico . Centro de Investigaciones de Quintana Roo(CIQRO) and Program of Studies in Tropical Conservation, Uni-versity of Florida, Chetumal, Quintana Roo, Mexico : 175-213 .

Reid, J. W., 1991 . The neotropical genus Potamocaris Dussart(Copepoda: Harpacticoida: Parastenocarididae), with descrip-tions of two new species. J . Crust. Biol . I 1 : 463-472 .

Reid, J . W., 1992 . Taxonomic problems : a serious impediment togroundwater ecological research in North America . In: J. A .Stanford & J . J . Simons (eds), Proceedings of the First Inter-national Conference on Ground Water Ecology. American WaterResources Association, Bethesda, Maryland: 133-142 .

Reid, J . W., 1994a. The harpacticoid and cyclopoid copepod faunain the cerrado region of central Brazil . 1 . Species composition,habitats, and zoogeography. Acta Limnol. bras . In press .

Reid, J . W., 1994b. The harpacticoid and cyclopoid copepod faunain the cerrado region of central Brazil . 2 . Community structures.Acta Limnol . bras. In press .

Reid, J . W. & T. Ishida, 1993 . New species and new records of thegenus Elaphoidella (Crustacea: Copepoda: Harpacticoida) fromthe United States . Proc . biol . Soc . Wash . 106 : 137-146 .

349

Reid, J . W. & G . G . Marten, 1994. The cyclopoid copepod (Crus-tacea) fauna of non-planktonic continental habitats in Louisianaand Mississippi . Tulane Stud. Zool . Bot. In press .

Stevens, G. C . 1989 . The latitudinal gradient in geographical range :how so many species exist in the tropics . Am . Nat . 133 : 240-256 .

Strayer, D ., 1988 (1989) . New and rare copepods (Cyclopoida andHarpacticoida) from freshwater interstitial habitats in southeast-ern New York . Stygologia 4 : 279-291 .

Turner, J . T., 1981 . Latitudinal patterns of calanoid and cyclopoiddiversity in estuarine waters of eastern North America . J . Bio-geogr. 8 : 369-382 .

Wilson, M. S . & H. C . Yeatman, 1959 . Free-living Copepoda. In :W. T. Edmondson (ed .), Ward & Whipple's Fresh-water Biology,2nd edn . J. Wiley & Sons, New York : 735-861 .