KIRK O. WINEMILLER. Ecological Divergence and Convergence in. Freshwater Fishes. Strong relationships between basic fonn and ecological function in fISh-.
KIRK O. WINEMILLER
. EcologicalDivergence and Convergencein FreshwaterFishes Strong relationships between basic fonn and ecologicalfunction in fIShes allow the comparative study of ecological relationships using morphological features. Within-fauna variation and between-fauna similarities of ecomorphological characteristics of freshwater fish assemblagesfrom five regions around the world were compared and contrasted. Ecomorphologicalfeatures allowed identification of a number of ecologically convergent spedes from different regions. Based on a relative scale of convergence,tropical fish assemblagesexhibited a greater degree of ecological convergence than temperate assemblages. The ecomorphological comparison supports the view that biotic interactions have a greater relative influence on evolution in the tropics compared with temperate regions.
Figure1. The bodyshape.posidonoffins. and nwuth structure of afish influenceits ecologicalperformance.Trout possessa generalited nwrphologythat allows them to usethe endre water columnand a wide variety offood itemsin habitats that contain reladvelyfew compedngspecies. PAlNTING BY WALTER A. WEBER Q NGS
308
IOLOGISTSAND POUCYMAKERSARE RAONG
the clock to document
and preservebiological diversityin the faceof a growing global human population and alterationsof naturalhabitats.Given the magnitude and rapid pace of changesto natural ecosys, biologists are challengedwith the taSkof identifying essentialfeaturesin the organizationof biologicalcommunities. Notwithstanding the inherent uniquenessof different geographical regionsand the evolutionaryhistoriesof their flora and fauna,the recognition of commonfeaturesamongcommunitiesand the speciesthat comprise them is sometimespossible.This study contributesto our understandingof biodiversity by further examining the ecologicalcharacteristicsof natural freshwaterfish communitiesfrom around the world. One of ecology'sgreatestchallengesis to explain patternsof regional speciesdiversity as well as the ecological,morphological,and behavioral variation among and within populations. Patternsof ecologicaland morphological diversification are of interest to both ecologistsand phylogenetic systematists.Systematistsuse interspecificvariationas the raw material for constructing phylogenies. Ecologists would like to know if interspecificvariation in a given trait arisesrandomly during evolutionary divergencefollowing speciation, or whether this variation is correlated with ecological function. This difficult task is further complicated by unique events.Traitsadaptivein a particular ecosystemmay be neutral or maladaptivein a new environment. If a maladaptivetrait is genetically correlatedwith one or more strongly adaptivetraits, then it might persist in the population for many generations.In one form or another,evolutionary biologistsand ecologistsseekto identify,interpret, and model patterns of functional (adaptive)variation.21Similaritiesin patterns of individual, population, and community-levelvariation amongdifferent faunas provide evidencethat, in many cases,the samedeterministic processes organizebiological systems. Biological convergenceis the independentevolution of the samefeature (physiological,morphological, ecological,etc.) within two divergent phylogenetic lineages. Divergence is the evolution of dissimilar traits betweenclosely related lineages.Remarkableexamplesof morphological and ecological divergence are well-known in vinually all higher taxa. Examples from the independent adaptive radiation among marsupial mammals of Australia and eutherian mammals of the other continents appearin most introductory biology textbooks.Convergence of ecological nichesis seenin rodentsand marsupialmice; shrewsand marsupialinsectivores; and eutherian canines and marsupial wolves. The bony fishes NATIONAL GEOGRAPHIC RESEARCH &. EXPLORAllON
8(3):308-327; 1992
(Osteichthys) are a much older and speciosephylogeneticlineageand as might be expected,exhibit numerous examplesof evolutionary convergence throughout the world (Figure 1). Within the Characiformes, Curimata (=Steindachnerina) argentea is an epibenthic mud-feeder; Hydrocynusvittatus is a large, roving midwater piscivore;Metynnisargenteusis a midwater planktivore/granivore;and Charaddiumfasciatumis a small, bottom-restinginvertebrate-picker.Within the PerCidae, Etheostoma chlorosomumis a small, bottom-resting invertebrate-picker; and Perca flavescensis an epibenthic and midwater insectivore/piscivore. A remarkable convergence of body form and ecological function has occurred betweenthe phylogeneticallydistant Characidiumand Etheostomaspecies (cylindrical body with flattened ventrum, broad pectoral fins, pelvic fins locatedanteriorly;subtenninal mouth, etc.). Despitethe number of instancesof remarkableconvergencethat can be identified within most large taxonomic groups (Figure 3), the convergencephenomenonis difficult to study quantitatively;This is especiallyso for small, closely related groupings. Our ability to recognizeevolutionary convergenceis entirely dependenton knowledgeof phylogeneticrelationships. Becausewe usually have more confidence in our phylogenetic groupings at broader taxonomic scales,ecological convergencecan be identified with greaterease.Within smaller and more recentphylogenetic lineages,it is often difficult to distinguish divergenttraits from convergent traits. In fact, a great deal of the methodology of modern phylogenetics CORRESPONDENCE seeksto identify the suite of traits that is uniquely divergent versus the suite that is convergent.2Phylogeniesare basedon the information contained in uniquely divergent (derived) characteristics.Convergenttraits are seen as potentially confounding characteristicsin phylogentic constructions. Among closely related taxa, the distinction between derived and convergent traits is sometimesunclear and only becomesapparent after phylogenetichypotheseshavebeengeneratedand tested. Here I present results from a comparative study of morphology and ecologyof freshwaterfish assemblages from five widely separatedregions around the world. Study sitesspan a latitudinal gradientfrom Alaska (650 N) to the neotropics (90 N), and a tropical longitudinal gradient from Central America (830W) to Africa (230E). Like many taxonomicgroups, freshwater fIShesshow a strong latitudinal gradient in speciesrichness, with the highest regional diversity appearing in the neotropics. R. H. Lowe-McConneW5counted> 1300 freshwaterfish speciesfor the Amazon River basin comparedwith 192 for all of Europe.Sincethat time, new discoverieshave causedmost estimatesfor South American fIShesto more than double, while the record for Europeanspeciesremains essentially unchanged.Whereas climatic and biogeographicalhistory are probably the primary underlying agents that produce global patterns of regional diversity;the basicmechanismsthat fostercoexistenceof largenumbersof speciesin tropical faunasare open to debate.The extent to which assemblagesfrom different regions are organizedin the samemanner indicates the degreeto which detenninistic processesregulatethe populations that comprisecommunities.33Moreover,the relativeamount of ecologicalconvergenceamong taxa from different regionsshould indicatethe strengthof KIRK O. WINEM1U.ER, assistant professor. similar forms of directional selection in relation to random evolutionary Departmentof Wildlife and Fisheries changeand evolutionary stasisdue to geneticconstramts.Here I contrast Sciences. TexasA&M University. College patterns of morphological divergencewithin the five local fISh assemStation.TX 77843-2258.
I am preparing a report on patterns of resource utilization and guild organization among diversefish assemblagesin Central and SouthAmerica, North America and Africa. In the interest of communicating with a diverse scientific audience,I have attempted to make the analysis fairly straightforward. This is sometimesdifficult to achievewith numerical analysesaimed at revealing temporal trends within speciesassemblagescontaining 30 to 70 species.
310
RESEARCH &. EXPLORAnON
8(3); 1992
Curimata
Hydrocynus
Metynn;s
Characidium
blages. A substantial literature illustrates the correlations between a number of basic morphological features of fishes and ecological performance (summarized in P:W Webb21),and morphology has been used successfully as a surrogate for ecology.6-8.11,20.26.28.32 In addition, I compare the relative degree of ecomorphological convergence between fish species from different regional faunas.
Etheostoma
~
Figure 2. Phylogenyshowingevolutionarydivergencr.within chtuadform and perdform fishes,as well as ecologicalconvergence betweenthe lebiasinidgenusof small, bottom-resting.invertebrate-pickers, Cbaracidium (C. fasciatum,South AmtTica),and thepercidgenusof small, bottom-resting.invertebrate-pickers, Etheostoma(E. chlorosomum,North America).
Methods SAMPLE COLLECTION Each of five study sites was sampledon at least two separatedates,and most locations were visited numerous times as part of long-term field studies.29-31 Only numerically dominant specieswere used for the morphological analysis.Dominant speciesare defined in this study as the most common speciesat a site that (by number of individuals), when summedby order of rank. formed 99% of all individual fIShescollected over the full samplii1gperiod. Rare specieswere defined as those comprising the 1% tail of smallest relative abundance contributing to the numericaltotal for a site. Whereasthis criterion for assemblagemembership could excludea few rare, but perhapsstrongly interactive, community elements,it was designedto eliminate most of the rare fugitive and transientspeciesthat were essentiallynon-interactive componentsof the coreassemblage (Table1). Two types of lowland aquatic environments-streams and backwaters-were sampledin eachof the following study regions:Alaska (North America), Texas (North America), Costa Rica (Central America), Venezuela(South America), and Zambia (Africa). This paper compares assemblage patterns of morphological and ecological divergenceamong ECOMORPHOLOGY OF FRESHWATER FISHES : WINEMILLER
311
FAMYLY (commonname) SEWARD PENINsUlA.
FAMIL Y (commonname) WESTERNPROVINCE,ZAMBIA
ALASKA RIVERS BACKWATERS TOTAL
spp.
spp.
6 0 0 1 0
2 1 1 1 1
SALMONIDAE (salmon.whitefishes) EsocIDAE
(pikes)
UMBRIDAE (bI8ckIIshes) CornDAE
(sc:uIpiDS)
GASTEROSTlIDAE (sdckIebIcks)
~ 7 0
No. GENERA No. DoMINANT SPEaES No. RARESPEaES
spp. 6 1 1 1 1
6 6 0
8 10 0
CREEK MORMYRJDAE (dcpb8nt aoscs) HEPSErIDAE (African pike) CHARAOOAE (teuu) CITHARIN1DAE (A&fcandanas) CYPRINIDAE (minnows) ScHIlBElDAE
MOCHOKIDAE ~ CYPRINOOONTIDAE ClOlUDAE ANABANTIDAE
NEWlON
COUNIY,
PETROMYZONIDAE (lamprey) CoUPEIDAE (sb8ds) ESOClDAE (pikes) CYPRINIDAE (miDnOWS) CATOSTOMlDAE (suckers) ICTALURIDAE (at6sbcs) APHREDODERIDAE (pirate perds) CYPRlNOOONTIDAE (kiUIfishes) (liftbearen)
ATHERINIDAE (sIlYasjdcs) CENTRARanoAE
(sunfishes)
PERaDAE (dartas) No. GENERA No. DoMINANT
SPEOES
No. RARE SPECIES
BAyOU
1 1 1 6 2 2 1 1 I i..
TOTAL
0 0 0 6 '1 0 1 1 1 0 3 1
6 3
1 1 1 9 '2 2 1 2 .1 1 7 3
8 13 0
18 26 0
19 31 0
1
TORTUGUEROPARK, COSTA RICA CREEK CHARAODAE(1£1ras) PIMB.oDlDAE (at6sbes) CYPRlNOOONTIDAE (kjIIIIIsba) POEauIDAE (ltYebams) ATHERINlDAE~) SYNGNATHlDAE(pipe6sbcs) POMADASYIDAE
Cvprinodontiformes Atheriniformes
Atherinidae (2/2)
Gasterosteiformes !I
Syngnathidae (1/1)
SvnRnathiformes Svnbranchiformes
Percoosiformes CvDI'inifDl'Ines
Characlformes
Scorpaeniformes Cenb'an:hidae(J/7) PelCklae(3/3) POOIadasyidae (1/1) Lutjanidae (1/1) Centroponidae (1/1) Ochlidae (11/34) Anabantidae (1/1) Eleotridae (3/4) Gobiidae (2/2) Mastacembelidae (1/1)
Salmonidae (4/5) Esocide(1/2) Umbridae (1/1) Aphredoderldae (1/1) Cyprinidae (4/17) UIosDnidae (2/2) OIaraddae (2W22) Curlmatidae (1/1) Gasterope\ecidae(1/1) lebiasinidae (3/3) Prochilodontidae (1/1) Cidlarinidae (1/2) GymfX)tidae (1/1) StemapYlidae (1/1)
PefCiformes
Siluriformes -
Pleuronectifonnes SoIeIdae (2/2)
number of closely related species that were actually less similar morphologically to the target species than its morphological nearest neighbor (N) divided by the total number of possible species pairings (P). P was equal to 158 for the first nearest neighbor, 157 for the second, and so on. The convergence index (NIP) was equal to 0 if the nearest neighbor was actually the most closely related taxon, and the index equaled 1.0 if the nearest neighbor was the most distantly related taxon in the entire data set. BecauseI did not distinguish degreesof relatednessbetween specieswithin a genus or genera within a family, any bias due to lack of true phylogenetic information was in the direction of no convergence. As a result, the convergence test is very conservative and slightly underestimates the magnitude and frequency of ecological convergences.
-
ktaluridae (1/2) PImelodidae (3/4) Auchenipteridae (1/1) Trichomycteridae (1/1) Aspredinidae (1/1) Callichthyidae (2/4) loricariidae (~) dariidae (1/1) Schllbeidae (1/1) Mochokidae (1/2)
Figure4. PhylogenyfoT 160fish species from Alaska, Texas,Costa~ Vmez:uela,and Zmnbia wed in the morphologicalanalysisof ecological divergenceand convergence(higher divisionsbasedon NelsonIB).
ECOLOGICAL DATA Information on feeding habits of ttopical fishes came from earlier longterm studies at the Venezuelan, Costa Rican, and Zambian sites.29-321nd refer-
-
Wrdn Diet was characterized by volumetric analysis of stomach contents based on large samples of formalin-preserved specimens. Those data are summarized here in the form of basic ttophic niches: algivore/detritivore, omnivore, invertebrate-feeder, invertebrate/fish-feeder, piscivore. The characterizations of basic trophic niches for Texan and Alaskan fIShes were based in part on information in K. D. Carlander.3.4
Results ASSEMBLAGE COMPOSITION Each of the study regions is dominated by different families (Table 1). Salmonids(salmon, grayling, whitefish) are the major componentsof the ECOMORPHOLOGYOF FRESHWATERFISHES: WINEMILLER
317
~
0.60
0.40
0.20 0.00
0.15 0.10 0.05 0.00
Figure 5. Distribudon of spedesnumerical relative abundanceby rank for five lowland backwaterand floodplainfish assemblages.
0.16 ~, 0.12 .~
0.08
"to "ii
0.04
rC~tiiiWI;i
~ VI .!!
0.00
~~-;."
~
0.20
:"~':~,'J~{;:!;:,!; ""C'-""""'-;;;-
V)
0.15
".u,,~.
::1ig~ ~ilt.~~:j;,:
-',
0.10 0.05
0.00 0.12
~~
0.08 0;04
0.00 SpeciesAbundance Rank
Alaskanassemblages, and cyprinids (minnows)and centrarchids(sunfishes) dominate Texan assemblages. In the tropics, cichlids and poeciliids Give-bearers)dominate CostaRicanassemblages; characids(tetras,piranhas) and catfishes(silurifonns) fonn the largestcomponentof Venezuelan assemblages; and cyprinids and cichlids dominateZambianassemblages. Within a habitat type (channelor backwater),assemblages show a strong latitudinal gradient in speciesdiversity with the highest diversity occurring in Venezuela.32 Richnessat the genusand family levelsalso showed strong latitudinal gradients among the five regions,but diversity at the ordina1levelwas not associatedwith latitude (Alaska-5 orders,Texas-9 orders,CostaRica-7 orders,Zambia-6 orders,Venezue1a-6orders). In a1llD assemblages, distribution of relativeabundanceamongspecies was strongly skewedin favor of uncommonspecies(Figure5). In terms of both individuals and biomass,relativelyfew speciestended to dominate eachfish assemblage. With few exceptions,numericallydominant species 318
RESEARCH & EXPLORAnON
8(3); 1992
~
400
200
0
Figure6. Di.stribudonof spcdes standard lengths by rank for five lowland backwater tmd
-=~ ;;;J~1i:
l~;I:
"~~Et
,,=-,- .
~C.!'II}i~""
6(X)
I
".J:.)r_;~c" " ;;iJii~~. E::":~.~ :J;~:,,~:I,~:~
Iii
floodpl4in fish GSStmblagtS (tach spedes standard length is the maximum recorded among all individuals colltcted at a silt).
300
:. "~',!t.-c
)~i~?:;JI; !if,
1~~:,;~f:;~;':
:!~*':;~g:::!
.
Mar3~ venezuel~;:'
I
.'t~ ,
J,:.:I ";ic~1
'".t
rj]~~~~~~~ 10
8t1
I
600
I
300
I0 Specieslength Rank
fed near the base of the aquatic food web (e.g., detritivores, algivores, gr.miVOl'ts, omnivores, planktivOl'ts). The predatory nonhero pike (Esax ludus) was the most abundant species in the Alaskan backwater sample. More than for other sites, the relative abundance figures in the Alaskan backwater sample were probably biased to some extent by the collecting methods (dip-netting in shallows, hook and line in depths). The Texas bayou sample was dominated by minnows (Notropis venustus, N. texanus, N. volucellus), mosquitofish (Gambusia affinis), and longear sunfish (Lepomis megalotis). A tetra (Astyanax fasciatus), predatory cichlid (Cichlasoma loiselld), eleotrid (EleotTis amblyopsis), and two algivorous live-bearers (Phallichthys amatt'S, Poedlia gilli) were most numerous in the Costa Rican backwater sample. The Zambian floodplain sample was dominated by a minnow (Barbus paludinosus), two catfishes (Schilbe mystus, Synodontiswoosnami), a killifish (Aplochdlichthys johnstoni) , and two her-
bivorous cichlids (1ilapia rmdalli, 1: spamnanO.The most numerousfishECOMORPHOLOGYOF fRESHWATERfISHES : WlNEMIliER
319
~
l!;;~~~~;,~£
~ ~J;;~
Figure7.
I
Results of principal components analysis based on 30 morphological characters and 160 fish spedes from five lowland backwater fish assemblages.The first PC axis modeled 24% of the total morphological varitJtion (eigenvalue=7.03) and the second axis modeled 14% (eigenvalue: 4.18). Vabal interpretations of the dominant variable loadings appear
;{~
;:f;'*'l~
belowtheaxislabels.
*1~!~:
-8~, " ...
-10
In highly variable environments, the advantages of a mo1phological specialization may only be perceived during a very limited period when resourcesare less abundant, population density is higher, or competitors are more abundant CORRESPONDENCE
320
.,,"4""'" ,."".~ " ~.".,4:'
~B~i~~;;ti, -s
0
5
10
es in the Venezuelanswamp included two small characids(Ctenobrycon spilurus, Odontostilbe pulcher), a mud-feedingcurimatid (Curimata argentea),a small callichthyid catfish(Corydorashabrosus),and an omnivorous cichlid (Aequidens pulcher). ECOLOGICAL DIVERGENCE The shapeof species-lengthdistributions (maximumstandardlength) was similar among backwatersites (Figure 6). Small and intermediate-sized fishesdominated all five assemblages. The averagesize of fIShesdid not differ significantly among backwater assemblages,except that Alaskan fisheswere larger than fishesfrom the other four regions.32The largest speciesin the comparativestudy was the northern pike from the Alaskan assemblage(750 mm). Most of the smallestadult fisheswere characids, minnows, and killifishes from the Zambianand Venezuelansystems.The African minnow (Barbushaasianus) attaineda maximum size of 17.3mm; the largest specimen of the African killifISh (Aplocheilichthyshutereaui) was 20.0 mm; and the largest specimen of the benthic citharinid (Hemigrammocharax machadoi)was 25.0 mm. Among Venezuelanfishes, the tetra (Creagrutussp.) reachesonly 28.0 mm; the catfISh(Corydoras habrosus)reaches25.0 mm; and the dwarf cichlid (Apistogrammahoignei) attains 30.0 mm. Most thesesmall fishes have shon life spans ranging from severalmonths to just over a year.In most instances,thesediminutive fishesspawn multiple clutchesof only a few to >100 small eggsduring the annual spawning period. The largestfIShesat all five sites have batch fecundities of tens or hundreds of thousands of eggs and synchronousspawningduring relativelyshon seasons.29 Figure 7 summarizesresultsfrom principal componentsanalysisof ecomorphological variation in the five backwaterfish assemblages.For an extensivestatisticalanalysisof variation in morphologicaltraits associated with ecological performance,seeWinemiller.32Assemblagescontaining fewer speciesat higher latitudesshow lessmorphologicalvariation (i.e., their speciescluster nearthe centerof multivariatemorphologicalspacein RESEAROi& EXPLORAnON 8(3); 1992
Small arthropods, seeds,filamentous algae H~
Ceratolxanchia
Hemigrammus
-',
V\
Fishscaies ExfXkNJ
Fishes 0Iara.- Genycharax
V Shearedflesh ~a.sa/mus
Aquatic plants ..",
\
Schizodon ")
';1"
~
Alpe, sponges, Invertebrates ~
L~us
"::j
~;/
Figure8. Examplesof adaptivedivugence in toothrrIO7phorogy amongSouthAmmam charaddand anostomidfishes (Charadformes).
ECOMORPHOLOGY OF FRESHWATER FISHES : WlNEMIUER.
DRAWINGSBASEDON GtRy (1977)
321
Thoracocharax stellatus
Gephyrocharax va/enciae
Figure9. Adaptive divergences in body form relative to distribution in the water column and swimming style in small. omnivorous, pool-dwelling charadd and gasteropelecidfishes (Charadformes) of South
America.
Aphyocharax alburnus Astyanax bimaculatus Popte/la orbicularis
Creagrutussp.
dwellers have fairly symmetricaldorsal and ventral proffies and terminal mouths (e.g., Asytanaxbimaculatus).Fusifonn fishes (e.g., Aphyocharax albumus)are proficient in dashingafter food particlesthat lie severalbody lengths away; however, they suffer a trade-off in positional stability and ability to perfonn sharp turning maneuvers.In contrast,deep-bodiedfishes (MetynnisaJgenteus)can turn sharply and position themselvesin the water column with great accuracy;However, the deep-bodymorphology carrieswith it a trade-off in proficiency for rapid straight-line swimming. Extreme forms of the deep-bodiedmorphology are conspicuousin pelagic fishes of tropical freshwaters,but are essentiallynonexistent in pelagic freshwaterfishesof the temperatezone. Most of the deep-bodiedmidwater fishes of the tropics are planktivores or fruit- and seed-eaters. Examplesamong the neotropicalCharacidaeinclude the giant pacus(e.g., Colossomamacropomum),smaller silver dollars (Mylossoma,Metynnis, Myleus spp.), and tetras (Tetragonopterus, Gymnocorymbus spp.). During certain times of the year,thesefishescompetefor seeds,fruits, and terrestrial arthropods that drop or are blown into the water. There is very little aquatic primary and secondaryproduction in the nutrient-poor aquatic systems inhabited by many of these fiShes. In such systems, I have observedlarge schools of Metynnissp. frantically snatchingup tiny adult midgesthat were trappedon the water'ssurfaceduring the previousnighL Thesefeedingfrenziesareintenseand short-lived as the midgesaredepleted in a period of severalminutes. Similarly, the robust, deep bodies of schooling piranhas (Pygocentrus spp.) are well adaptedfor quick maneuvering at close range during feeding frenzies.In contrast, the long cylindrical bodiesof pike-like predatorsare efficient for swimming by meansof brief, rapid bursts along a straight-line trajectory; I placed eachof the speciesof the five backwaterassemblages into five generaltrophic categories(detritivores/algivores,omnivores,invertebratefeeders,piscivores,invertebrate-feederstpiscivores) basedon dietary data (volumetric proportional usageof general food categories).Specieswere alsoassignedto five habitat categories(benthic, epibenthic,midwater,surface,vegetation) basedon the field collection records'of fishes captured from different habitatsand pool zones.The relativefrequencyof speciesin 322
RESEAROi 67.EXPLORATION 8(3); 1992
the five n-ophic categories showed some general similarities across regions (Figure 10). Except for the codominance of invertebrate-feeders and omnivores at the Venezuelan site, invenebrate-feeding was the most common n-ophic guild irrespective of the region. Algivores/detritivores, pisciVOTes,and species that, as adults, consume a mixtUre of invenebrates and fishes were also present in all regional assemblages. Nevertheless, there were significant differences in the relative proportions of trophic categories represented in regional fISh assemblages (X2 = 34.78, df- 16; p< 0.005). Omnivores (diets consisting of a mixture of 8lgae, seeds, fruits, detritus, insects, crustacea) were just as abundant as invertebrate-feeders in the Venezuelan assemblageyet were entirely absent from the two temperate zone assemblages. Fish assemblages from higher latitudes were more heavily skewed in favor of invertebrate-feeders, whereas n-ophic categories tended to be more evenly apportioned with decreasing latitude (Figure 10). Habitat categories exhibited fewer interfaunal differences than n-ophic categories (x2
-
12.62, dj-16, p= 0.70). Again, the Venezuelan
backwater assemblagetended to have more even distribution of species within the five categories than the high-latitude assemblages.The majority of AJaskan fishes were midwater forms, and none were surface-dwellers.
Benthicfishesdominated theVenezuelan swampassemblage. ECOLOGICAL CONVERGENCE Accolding to the operational definition of ecomorphological convergence (convergenceindex values ranging from 0 to 1.0), convergencewas seen in all five regional assemblagesat low frequencies (Figure 11) and was usually not extreme. Most convergence index values were small (0< index value
~I' .,w,)_c.,. .
i,.~,I'j"i,c-~;"f)![;~""
..
~~~.1::~;;;'"!i~..
"';f,"'I"~"i;" ;J'J!,.~;;;'1~"""',r"
c ;r;~.1!","~"#.""",,
,,'.0
~ii!1
G)
,.. 0 6 ~
":i:'fQ j 0:4
yt
.. :;~ ;,;;,.
".. Algae/delt.
~
-- 0Im'-
Fishes
figure 10. frequndes of spedesassociated with Jive general trophic categories(top) andJive habitat categories(bottom)for backwaterfish assemblagesin five biotic regions.
0.2
~;; 0.0
Trophic Category
0.6
.. . . .
Alaska,6 species Texas,26 species CostaRica.30 species Zambia,33 species Venezuela,43 species
.~\
G.4
-"~:~.
I.-:iti~-Surface Mi6NaIeI HabitatCategory ECOMORPHOlOGY OF FRESHWATER FISHES : WINEMIllER
323
The ability to shift from a restricted diet to one that incorporates several alternative foods is obviously adaptive when these alternative resourcesare seasonallyabundant. CORRESPONDENCE
0.5). Eel-like fishes (Ichthyomyzon gaga, Synbranchus mannoratus, Afromastact:mbt:lusfrmatus) exhi;bited extreme convergence (index value -1.0). The spiny eel, Afromastacembelus (Perciformes), is genetically more similar to perches, sunfIShes, and cichlids than to other eel-like fishes. The extremely elongate African catfish, Clarias theodorae,is more similar in morphology and ecology to the eellike fishes than it is to most other ~tfishes. A taxonomically diverse group of small, surface-feeding insectivores are ecological equivalents (e.g., Alfaro cultTatus [PoeciliidaeI, J\plochdlichthysjohnstoni [Cyprinodontidae I, Gephyrocharaxvalendat:[Characidae]). A number of instances of extreme ecomorphological convetgence were identified even at the family level. Within the family Cichlidae, the large predatory guapote (Cichlasoma dovii) was more similar to predatory African cichlids (Serranochromismacrocephalusand S. robustus) than to more closely related neotropical Cichlasoma species (Figure 3). Similarly; the predatory, vegetation-dwelling cichlid Cichlasoma loise-lId (Costa Rica) was more similar to the African cichlid Htmichromis elongatus and the Nonh American sunfish Lepomis cyandlus than to most other Central American Cichlasoma.Within the Cyprinidae, several African Barbus sp. (e.g., B. paludinosus) matched most closely with North American Notropis sp. (e.g., N. atrocaudalis) with similar ecological niches. Numerous other examples of pairwise ecomorphological convergence could be cited among the data that yield the nonzero values in Figure 11. Among Alaskan fishes, extreme instances of convetgence with Species from other faunas involved the sit-and-wait/stalking piscivore Esox lucius (Figure 3). In general, high convergence index values (>0.5) were more frequent among tropical speciesthan temperate species(Figure 11).
Discussion
.... ........................................ .. ... . . . .. . . Comparisonsamongfive regionalfish assemblages yielded patternsof latitudinal taxonomic diversity that are consistentwith most earlier studies involving large groups.e.g.,n Given the greaternumber of speciesin the tropics, it is perhapsnot surprisingthat greatermorphologicaland ecological diversity is observedin tropical fIShesthan in temperatefishes. In a separateanalysisbasedon the samespecies,I concluded32that the statisticalproperties of this greaterecomorphologicalvariation in tropical assemblagessupport an interpretationof evolution in responseto deterministic forces. Competition for food resources,either directly or indirectly via microhabitat selection,is probablya major sourceof natural selectionon ecomorphological characteristicsin the tropics. Patterns of divergence within the Texan fIShassemblage were generallyconcordant with those observedin tropical fIShassemblages, which suggeststhat deterministic forcesare alsoat work in species-richtemperatefaunas. Comparedwith tropicalfaunas,the lesserdegreeof taxonomic and ecological diversificationin temperatefaunasmost likely results from greater rates of speciesextirpations in temperateregions on a geological time scale.Most biogeographers agreethat the habitat chang"es associatedwith the glacial epochswere more severeat higher latitudes. In addition, the 324
RESEAROI&: EXPLORAnON 8(3); 1992
Figure 11. Frequenciesof spedespairs showingvarious degreesof ecomorphologicalconvergence basedon the relative convergence index. N~ero convergence values(valuesare groupedat intervals ~n the x-axis) indicates that at leastone closephylogenetic relative was lesssimilar ecomorphologicallythan the ecomorphologicalnearestneighbor. Convergencevalues>0.2 indicate that >20%of closephylogenetic relativeswere lesssimilar ecomorphologicallythan the nearest neighbor(convergenceindex definedin text). ~ c "t: "to 0~
~
.~ VI 0
. . . . .
NN1 NN2 NN3 NN4 NNS
seasonalchangesin environmentalconditions are more extremeat higher latitudesand altitudes,but the ecologicaland evolutionaryimplications of these proximate fluctuations can be debated.Seasonalinterruptions of density-dependentenvironmentalconditions occur in tropical as well as temperatesettings.29,JO All natural communities are influenced by both biotic density-dependentand abiotic density-independentfolCes,but the relative influenceof eachvariesgreatly from one geographicalsetting to the next. The analysisof fISh ecomorphologicalpatterns32supports the ECOMORPHOLOGY OF FRESHWATER FISHES : WINEMILLER
325
Just as mostfishes continue to grow throughout their lives, ecological performancefrequently exhibits major changesover the lifespan. Larval fishes generally feed on zooplankton and other microscopic organisms. Wefind the greatest morphological diversity and ecological diversity among adult size classes,and that is why I restricted my comparative analysis to adult fishes. CORRESPONDENCE
326
general view that biotic interactions have a greater relative influence on evolution in the tropics than in temperate and polar regions.s Ecomorphological convergence among phylogenetically divergent taxa provides powerful evidence for determinism in the evolution of species traits. If two divergent taxa can be shown to have evolved similar solutions for the same problem in different regions, we gain a measure of confidence in our inferences of adaptive functions and that at some level, a set of universal rules exists for the structuring of natural communities. Reports of convergent traits (e.g., fISh electroreceptio~12.15lizard toe fringes16) and ecologically equivalent species (e.g., fishes,24birds,1O.19.2S lizards2J) abound in the literature. The phylogenetic foundations for hypotheses of convetgenceare now receiving greater attention and integration with ecological research.2Morphological variation among homologous features at a micro-scale (osteology, musculature, ligaments, etc.) provides systematists with evidence of phylogenetic relationships. When subjected to intense scrutin~ many of these small-scale changes in morphology can be shown to cause significant shifts in ecological function; e.g., G. v: Lauder13 showed how small morphological changes in neuromuscular physiology result in differencesin feeding performance in sunfishes. The simple convergenceindex used in this study was designed to identify convergence in basic morphological features related to ecological function. This method requires knowledge of phylogenetic relationships. In practice this is never actually the case, because any phylogeny represents only one of several possible hypotheses of relationship. Evolutionary convergences are recognized when similarities in basic form and function emerge from different (analogous) structural components at the microscale. Parallel evolution occurs when two divetgent lineages independendy evolve the same featuresin response to similar selective environments. The convergence index cannot distinguish between parallel evolution and evolutionary stasis (lack of morppological differentiation in two independent lineages). As new morphological and biochemical data produce larger and more detailed phylogenies, new methods can be developed to test a variety of evolutionary ecological hypotheses. This study identified a number of convetgent speciespairs from different geographical regions. The analysisidentified many more instances of partial or weak convetgencesand numerous species that showed no ecomorphological convergencewith speciesfrom other assemblages.At the level of the species assemblage,morphological diversification was similar among the three regions of intermediate speciesdiversity. The Alaskan fish assemblage showed very litde interspecific variation in ecomorphology, and the speciose Venezuelanassemblageshowed greater variation than other sites. As a function of the physics of movement through a fluid medium, basic body shape strongly influences ecologicalperformance. In fishes,variation in body form correlates with variation in swimming behavior and partitioning of space within aquatic habitats. Feeding ecology is correlated with morphological features such as tooth shape, mouth size, and mouth orientation. Tropical fishes from species-richassemblagesdisplay the greatestvariety of ecological roles. Finall~ some morphological traits are associatedwith defense against predation (e.g., stout spines, cryptic coloration, mimicry) and reproductive biology (fin filaments, flashy coloration, nuchal humps). Tropical freshwater fishes appear to exhibit far greater diversification than temperate fishes in these features as well. RESEAROI61EXPLORAllON 8(3); 1992
REFERENCES
18. Nelson,j. S.: Fishesof thc world, 2nd ed. john Wiley &. Sons,NewYork; 1984. 19. Niemi. G.j.: Pattemsofmorphological evolution in bird generaof New World and Old World peatlands.Ecology 66:1215-1228;1985. 20. Page,L. M.; &. Swofford,D. L.: Morphologicalcorrelatesof ecological specializationin daners. Environmmtal Biologyof Fishes11:139-159;1984. 21. Pagel,M. D.; &. Harvey,P. R.: Recentdevelopmentsin the analysisof comparativedata. TheQuarterly~cw of Biology63:413-440;1988. 22. ~ E. R: latitudinalgradientsin speciesdiversity. Ammcan Naturalist 100:33-46;1966. 23. ~ E. R: Someintercontinental comparisonsof desenlizards. National GeographicResearch 1:490-504;1985. M. Sazima,I.: Similaritiesin feeding behaviorbetweensomemarineand freshwater fishesin tWotropical communities. JournalofFish Biology29:53-65;1986. 25. Schluter, D.: Testsfor similarity and convergenceof finch communities. Ecology67:1073-1085;1986. 26. Watson, D.j.; &. Balon.E. K.: Ecomorphologicalanalysisof fish taxacenesin rainforeststreamsof northern 9. Gtry.J.: Characoids of the World. Borneo.JournalofFish Biology25:371TFH Publications, Neptune, Nj; 1977. 384; 1984. 10. Karr.J. R; &:James,F. C.: £co27. Webb, P. W.: Bodyform,locomomorphologicalconfigurationsand convertion and foragingin aquaticvertebrates. gent evolution in speciesand communiAmcricanZoologistM:I07-120; 1984. ties. Cody, M. L &: Diamond.J. M., 28. Wikmmanayake,E. D.: editors: EcologycmdEvolutionof CommunEcomorphologyand biogeographyof a ides.258-291. BelknapPressof Harvard tropical streamfish assemblage: Evolution University, Cambridge.MA; 1975. of assemblage strUcture. Ecology 11. Keast.A.; &: Webb. D.: Mouth 71:1756-1764;1990. and body form relative to feedingecology 29. Wmemiller, K. 0.: Patternsof in the fish fauna of a small lake, Lake variation in life history amongSouth Opinicon, Ontario. Journal of the Americanfishesin seasonalenvironments. FisheriesResearch Boardof Clmada Oceologla81:225-Ml; 1989. 23:1845-1874; 1966. 30. Wmemiller, K. 0.: Spatialand 12. Kirschbaum.F.: Reproductionof temporalvariation in tropical 6sh trophic weakly electricteleosts:Just anotherexamnetworks. EcologicalMonographs ple of convergentdevelopment?Environ60:331-367;1990. mentalBiologyof Fishes10:3-14; 1984. 31. Wmemiller, K. 0.: Comparative 13.Lauder,G. V.: Neuromuscular~tspecies ternsandthe origin of trophicspeda1izatiom ecologyof Serranochromis (Teleostei:achlidae) in the Upper in fishes.SdDIa 219:1235-1237;1983. ZambeziRiver. Journalof FishBiology 14. Lee. D. S.; GUbert,C. R; &: 39:617-639; 1991. Hocutt, C. H.: Atlas of North Amcrfam 32. WmemUler,K. 0.: Freshwater Fishes. North Carolina State Ecomorphologicaldiversificationin lowMuseum of NatUral History. Raleigh; 1980. land freshwater6sh assemblages from five 15.l.owe-McConnell, R H.: Fish biotic regions. EcologyMonographs Communitiesin Tropical Freshwatm: Their 61:343-365;1991. DIstribution,Ecology,cmdEvolution. 33. Winemiller, K. 0.; &. Pianka, LongmanPress,London;1975. E. R: Organizationin naturalassem16. Luke. C.: Convergentevolution of blagesof desenlizardsand tropical6shes. lizard toe fringes. BiologicalJournalof the EcologicalMonographs 60:27-55;1990. Linne4nSocidy 27:1-16; 1986. 17. Mago, F.: Lista de IosFecesde V~ Oficina Nacionalde Pesca, Ministerio de AgricultUI2y Cria, Caracas, Venezuela;1970.
1. Bell-Cross,G.; &: Minshull,J. L: TheFishesof zimbabwe.National Museumsand Monumentsof Zimbabwe, Harare,Zimbabwe;1988. 2. Brooks, D. R; &: McLennan,D. A.: PhylogOlY,Ecology,and Behavior.University of ChicagoPress,Chicago,IL; 1991. 3. Carlander, K. D.: Handbookof FreshwaterFisheriesBiology,vol. 1. Iowa StateUniversity Press,Ames; 1969. 4. Carlander,K. D.: Handbookof FreshwaterFisheriesBiology,vol. 2. Iowa StateUniversity Press,Ames; 1977. 5. Dobzhansky,T.: Evolution in the tropics. AmericanSdcntist 38:209-221; 1950. 6. Douglas,M. E.: An ecomorphological analysisof niche packingand niche dispersionin streamfish clades.Matthews, W.J.; &: Heins,D. C, editors:Community cmdEvolutionaryEcologyof North Amerialn StreamFishes,141-149. University of OklahomaPress,Norman; 1987. 7. Gatt, A.J.Jr.: Ecologicalmorphology of freshwaterstreaD1 fishes. TulaneStudiesin ZoologycmdBotany 21:91-124; 1979. 8. Gat%.A.J.Jr: Community organization in fishesasindicatedby morphological featUres.Ecology60:711-718; 1979.
ECOMORPHOLOGY OF FRESHWATER FISHES : WINEMILLER
ACKNOWLEDGMENTS Numerouspe.sonsassistedin the field collections,and specialthanks go to L KeIso-Wmt:mi1ler, D.C. Taphom, LG. Nico, A. Barbarino,E. Urbina,J. Masinja, G. Milini, Mr. Sinda.W. Ritter, and M. Kelso.L Kelso-Wmemiller hasmy tremendousgratitUdefor assistingin measurementsof-manyfish specimens.I thank A. Brenkertfor assistancein data management.InstitUtional suppon abroad was providedby D.C. Taphom of Ia Universidadde los Uanos Occidentalesin Venezuela.H. Haug and E. Chamorro of el Serviciode parquesNacionalesde Costa Rica,and E. Muyangaand G. Milindi of the Departmentof Fisheriesof Zambia. Collectingand fishing pennits were obtainedfrom Ia DirecciOnAdministaci6n y Desarollopesquerode Ia Republicade Venezuela,el Serviciode Parques Nacionalesde CostaRica,the Depamnent of Fisheriesand National Commissionof DevelopmentPlanningof the Republicof Zambia,and the AlaskaDepanmentof Fish and Game.Fieldwork was fundedby the National GeographicSociety,Tinker Foundation,NSF DissertationGrant, and a Fulbright Grant for International Exchangeof Scholars.Oak RidgeNational Laboratoryis managedby Manin Marietta EnergySystems,Inc. under contract DEAC05-840R21400with the U.S. Departmentof Energy.
327
