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Home , Ammocrypta, Duskytail darter, Etheostomatinae, Etheostoma variatum, Glassy darter, Gulf darter

Evolution of Reproductive Behaviors in Percid Fishes

Lawrence M. Page

Percid fishes are freshwater deriva- iors of percids results in a better under- tives of a marine perciform, perhaps an standing of the relationships among anadromous serranid (McCully 1962; species. Collette & BaTna-rescu 1977). They ap- pear to be relatively recent (i.e., most evolved during the Pliocene or later) ACKNOWLEDGMENTS but have undergone a tremendous radi- ation in North America, where they I am grateful to an anonymous re- now comprise about 151 species in five viewer and especially to James D. Wil- genera. Among North American fresh- liams for constructive comments on the water fishes, only minnows (Cyprini- manuscript. I wish to thank B. M. Burr, dae), with about 225 species, are more D. A. Etnier, and W. C. Starnes for un- diverse. Together, percids and minnows published information on the spawning constitute almost half of the temperate habits of E. parvipinne E. (Nanostoma) North American freshwater fish fauna. spp., E. trisella, and E. (Catonotus) sp. In addition to being diverse groups, these fishes often occur in large popula- tions and are important in determin- TYPES OF ing the ecological characteristics of REPRODUCTIVE BEHAVIORS North American streams and lakes. Elsewhere, percids are present only in Accompanying the evolution of a temperate Eurasia, where there are 14 large diversity of percids has been the species in six genera. Two genera, evolution of a variety of reproductive Stizostedion and Perca, occur in both North America and Eurasia (Table 1). Several reasons exist for studying Table 1. — Percid taxa and their distributions. the reproductive habits of organisms. Among these are that (1) reproductive habits are inherently interesting; Taxa Number of Species Distribution (2) reproduction is that activity toward which all life processes ultimately are directed and, therefore, understanding Luciopercini its variations is important if we wish Stizostedion 5 Holarctic to protect or manage species; and (3) re- Etheostomatini productive characteristics provide in- Nearctic formation useful in estimating evolu- ca. 38 tionary (phylogenetic) history. Percids 7 Nearctic are especially interesting in this last Etheostorna ca. 103 Nearctic regard because, as a recent and diverse Romanichthyini group, transitions among their various Zingel 3 Palearctic types of reproductive behaviors remain Roman ichthys 1 Palearctic evident today. Reconstructing the evolu- tionary history of reproductive behav- Percinae 1 Palearctic Dr. Lawrence M. Page is an Ichthyologist, Sec- Perca 3 Holarctic tion of Faunistic Surveys and Insect Identifica- 4 Palearctic tion, Illinois Natural History Survey.

275 276 ILLINOIS NATURAL HISTORY SURVEY BULLETIN Vol. 33, Art. 3 strategies, and in the most advanced Courtship consists of an individual of states, parental care of the eggs. either sex approaching another indi- Among the 76 species of percids for vidual from behind or from the side which spawning behaviors are known, and pushing against it. The approached six types of behavior are recognized, fish either withdraws or, if sexually re- some of which can be subdivided fur- sponsive, makes quick darts forward ther, as discussed below. These six and upward. This increased activity types, named for the mode of egg- often elicits the attention of other indi- deposition, are termed (1) broadcast- viduals, and soon a compact group ing, (2) stranding, (3) burying, (4) at- forms, which periodically rushes for- taching, (5) clumping, and (6) cluster- ward and upward. Eggs and sperm are ing. released during a forward rush of ac- tivity (Ellis & Giles 1965). Spawning Broadcasting groups vary from two individuals to Broadcasting is the primitive mode several individuals of both sexes (Fig. of reproductive behavior among fishes 1). Eggs are adhesive for a few hours, and is retained in primitive percids. and they may adhere to rocks or plants Eggs and sperm are discharged in large for a short time; ultimately they fall to numbers, often in a frenzy of activity the bottom and into interspaces among involving several individuals. A coarse the components of the substrate (Fig. substrate, usually composed of rocks or 2), where they presumably are less ex- plants, is chosen to provide crevices and posed to (Colby et al. 1979). other hiding places for the fertilized S. marinum (Cuvier) and Percarina eggs. In its most primitive state, broad- demidoffi Nordmann appear to exhibit casting makes no other behavioral pro- similar, perhaps identical, behavior visions for the eggs, either before or (Berg 1949) although descriptions of after spawning. spawning are vague. Stizostedion vitreum (Mitchill) and Stizostedion lucioperca (Linnaeus) S. canadense (Smith) broadcast their exhibits a modification of this behavior eggs between March and June in in that eggs and sperm are broadcast streams and in areas of lakes with suf- over a circular pit previously con- ficient water movement to ventilate the structed by the male. The pit is lined eggs (Eschmeyer 1950; Nelson 1968). with gravel, shells, or plant material Spawning usually occurs in the even- (often roots) and is guarded before and ing (Ellis & Giles 1965) or at night after spawning by the male, who also (Eschmeyer 1950), and territories are fans the fertilized eggs (Kryzhanovshy not established (Ellis & Giles 1965). et al. 1953). Mating in this more special-

Fig. 1. — Stizostedion vitreum congregated on spawning grounds at Lake Gogebic, Michigan, 4 May 1948. From Esch- meyer (1950). (Photo pro- vided by the Institute for Fisheries Research, Fisheries Division, Mich- igan Department of Nat- ural Resources.)

September 1985 125 YEARS OF BIOLOGICAL RESEARCH 277

Fig. 2. — Eggs of Stiz- ostedion vitreum on spawning ground at Lake Gogebic, Michigan, 12 May 1948. From Esch- meyer (1950). (Photo pro- vided by the Institute for Fisheries Research, Fisheries Division, Mich- igan Department of Nat- ural Resources.)

ized, nesting broadcaster may be mon- rington 1947; Hergenrader 1969) and ogamous (Deedler & Willemsen 1964). P fluviatilus Linnaeus (Seeley 1886:27; Wheeler 1969:322; Treasurer 1981). It Broadcasters also may occur in Gymnocephalus cer- nua (Linnaeus), as described by Seeley Group A. over open substrate (1886:36) and Wheeler (1969:321), al- Stizostedion vitreum (Eschmeyer 1950) though some authors (e.g., Nikol'skii S. canadense (Nelson 1968) 1961:369; Muss 1978:161) discuss S. marinum (Berg 1949) spawning in Gymnocephalus without Percarina demidoffi (Berg 1949) mentioning egg strands. Group B. Spawn over male-constructed pit Stranders S. lucioperca (Kryzhanovshy et al. 1953) Gymnocephalus cernua (Seeley 1886) Perca flavescens (Worth 1892) 1886) Stranding P fluviatilus (Seeley Stranders have the unique habit of encasing their eggs in long gelatinous Stranding is probably a direct deriv- strands. A ripe female is followed by ative of broadcasting. The eggs become several males through beds of vegeta- encased in gelatin in the ovaries and tion (sometimes tree roots or debris) in when emitted remain part of a cohesive slowly flowing or standing water. The mass rather than becoming independ- males release sperm as she extrudes a ently scattered. The derivation of convoluted egg strand (Worth 1892; stranding from percid spawning behav- Treasurer 1981). The strand is gelatin- iors other than broadcasting is less ous, transparent, hollow, and arranged likely, because each is specialized in a in bellowslike transverse folds. When way that seems to preclude the evolu- first laid, the shape of the egg mass is tion of stranding. similar to that of the ovarian cavity For a female to put all of her eggs (Fig. 3), but eventually it stretches (Fig. in one highly visible basket, which 4) and may reach a length of 2.4 m and stranding certainly does, and then a width of 10 cm (Hardy 1978). Egg abandon them would seem to be a stra- stranding is known to occur in Perca tegy quickly selected against unless flavescens (Mitchill) (Worth 1892; Har- the eggs somehow are protected intrin- 278 ILLINOIS NATURAL HISTORY SURVEY BULLETIN Vol. 33, Art. 3

Ft■

Fig. 3. — Eggs of Perca flavescens encased in ovaries (left) and in gelatinous strands after being spawned (right). From Worth (1892). sically against predation and disease. surface of the substrate. In egg bury- Having toxic, or at least distasteful, ing the female works her body partially eggs would be an obvious strategy, but below the surface of the substrate and, observations by Seeley (1886:27) of with her genital papilla buried and a predation by "birds and various fishes" male mounted on her back, expels eggs on eggs put this method in doubt. (Fig. 5). The substrates usually used Treasurer (1983) reported low mortality are loose gravel, sand, or mixed gravel of perch eggs and attributed it to the and sand. Egg burying is characteristic improved ventilation and midwater of many , including all species position (thereby avoiding siltation) of of Percina for which spawning observa- the strand. tions have been published and many species of . Some egg buriers Burying are thought to be territorial (Winn Egg-burying behavior is similar to 1958), but other than the indirect pro- broadcasting except for the important tection associated with territoriality, distinction that the release of eggs oc- eggs receive no parental care. Among curs just below, rather than above, the darters, burying represents the primi- September 1985 125 YEARS OF BIOLOGICAL RESEARCH 279

Fig. 4. — Egg strand of Perca flavescens. From Pearse & Achtenberg (1921).

Fig. 5. — Egg-burying behavior. With a male mounted on her back, a partially buried female deposits eggs below the surface of the substrate. Eggs are fertilized as they are laid and then are abandoned by both parents.

A Fig. 6. — Egg-attaching behavior. (A) The female selects the site of egg deposition. (B) The male mounts the female and releases sperm as eggs are attached to plants. The eggs subsequently are abandoned. 280 ILLINOIS NATURAL HISTORY SURVEY BULLETIN Vol. 33, Art. 3 tive form of reproductive behavior; taching eggs to plants seems to involve among percids, it represents an egg- behavior identical to that of attaching hiding modification of broadcasting eggs to rocks; the substrate used is that behavior. which is readily available in the habi- tat. Eggs are abandoned and receive no Buriers direct parental care, although as in some burying species, territorial be- Percina (Alvordius) maculata (Petravicz havior may provide some protection. 1938) P (A.) peltata (New 1966) Attachers P (A.) notogramma (Loos & Woolcott 1969) Etheostoma (Etheostoma) blennioides P (Ericosma) evides (Page et al. 1982) (Fahy 1954) P (Hypohomus) aurantiaca (Howell 1971) E. (Nanostoma) zonale (Winn 1958) P (Cottogaster) copelandi (Winn 1953) E. (N) coosae (O'Neil 1981) P (Percina) caprodes (Winn 1958) E. (N) baileyi (Page personal observa- Etheostoma (Litocara) nianguae (Pflieger tion) 1978) E. (N) simoterum (Page & Mayden 1981) E. (Psychromaster) tuscumbia (Koch E. (N) duryi (Page et al. 1982) 1978) E. (N) barrenense (Winn 1958) E. (Etheostoma) tetrazonum (Pflieger E. (N) rafinesquei (Winn 1958) 1978) E. (N) sp. (Red Snubnose) (B. M. Burr E. (E.) variatum (May 1969) personal communication) E. (Doration) stigmaeum (Winn 1958) E. (N) sp. (Lowland Snubnose) (B. M. E. () juliae (James 1983) Burr personal communication) E. (N) rufilineatum (Stiles 1972) E. (Ioa) vitreum (Winn & Picciolo 1960) E. (N) camurum (Mount 1959) E. (Vaillantia) chlorosomum (Page et al. E. (N) bellum (W. D. Voiers personal 1982) communication) E. (Belophlox) okaloosae (Collette & E. (N) tippecanoe (Trautman 1981) Yerger 1962) E. (Fuscatelum) paruipinne (B. M. Burr E. (Villora) edwini (Williams 1976) personal communication) E. (Ozarka) boschungi (Boschung 1979) E. (Ozarka) cragini (Distler 1972) E. (0.) trisella (W. C. Starnes personal E. (Oligocephalus) spectabile (Winn 1958) communication) E. (0.) caeruleum (Winn 1958) E. (Oligocephalus) lepidum (Strawn 1956) E. (0.) radiosum (Scalet 1973) E. (0.) asprigene (Page et al. 1982) E. (0.) swami (Ruple et al. 1984) E. (0.) grahami (Strawn 1956) E. (0.) ditrema (Seesock et al. 1978) Attaching E. (Boleichthys) exile (Winn 1958) E. (B.) fusiforme (Fletcher 1957) Attaching behavior is a derived be- E. (B.) gracile (Braasch & Smith 1967) havior known among percids only in E. (B.) proeliare (Burr & Page 1978) the Etheostoma. The female se- E. (B.) fonticola (Schenck & Whiteside lects the site of egg deposition (presum- 1977) ably in some species within a male's E. (B.) microperca (Burr & Page territory), typically a plant or large 1979) rock, and with the male following her, elevates to the site. As she does so, the The presence of both egg-burying male follows and mounts, the two vi- and egg-attaching species within three brate, and eggs and sperm are released subgenera of Etheostoma (Etheostoma, (Fig. 6). Usually one to three adhesive Ozarka, and Oligocephalus) suggests eggs are released during each spawn- that egg attaching is derived directly ing act and are pushed by the female from egg burying and has arisen inde- onto a plant, rock, or other object. At- pendently in several unrelated groups (3) interruptedsupratemporalcanal, (4)incom- (black rectangles)are(1)25or fewerpored outgroup comparisons to ships amongspeciesof morphous character stateswereidentifiedby first dorsalfin,(6)brightorange venteronthe plete lateralline,(5)brightorange marginonthe breeding male, cephalus) whipplei lateral-line scales,(2)seveninfraorbital pores, distribution amongspeciesof ently alsohasarisenindependently September 1985 morphological synapomorphies(Fig.7). is inconsistentwiththedistributionof tain conditions(Petravicz1936;Page& among specieswithinsubgenera;its of darters.Infact,atleasttwospecies been observedtoburyeggsundercer- Mayden 1981).Eggattachingappar- which usuallyattachtheireggshave Fig. 7.—Hypothesizedphylogeneticrelation-

punctulatum (7)

heavily mottledbody.Synapo- and Ozarka. E. (Belophlox) Etheostoma (Oligo- Synapomorphies pall ididorsum 125 YEARSOFBIOLOGICALRESEARCH fricksium. Ozarka 0 (Radcliffe andWelsh),thesolemember [including also sellare 1976; Page1981)species on theverge of egg-clumpingandegg-clustering of .Ithasaflattened genital Swain, and species (Page&Swofford 1984).If shown tobeeggattachers. (Fig. 7)isaccurate, the onlyknownattacher, major significance ineffortstoprotect latter behavioral groups,itcouldbeof papilla (Knapp1976)similar tothose of thethirdmajorlineageinsub- and Evermann, dan andBrayton), dan andBrayton), bert], allofwhicheventuallymaybe Gilbert andSwain, Rafinesque, isamemberofthesecond Black), major lineage[including genus, isahighlydistinctive(Knapp are inthe and species ofthesubgenus However, itisinterestingthatthetwo Robison 1980).Independentderivation man), and known buriers known tocomparetheirdistributions relationship tooneanother. of thisbehaviorinthetwospecies eggs tovegetationinheadwaters(even same spawningrequirementsandbe- seepages) C. Starnespersonalcommunication).If E. boschungi E. cragini with aphylogenybasedonmorphology. weakens theargumentfortheirclose havior (Boschung1979;Williams& the phylogenybasedonmorphology behavior independentlyofoneanother. The factthat ing itinthesubgenus munication) wasamajorfactorinplac- their eggstoplants(Boschung1979; trisella boschungi, trisella The breedingbehaviorsoftoofew E. tetrazonum is foundtobelongoneof these must haveevolvedegg-attaching E. osburni Bailey andRichardsattach ( W. Gilbert buriesitseggs,but E. kanawhae E. which hasessentiallythe E. histrio C.Starnes,personalcom- Wall andWilliams

uariatum E. euzonum E. trisella E. blennius [E. variatum E. swannanoa E. thalassinum (Hubbs andBlack)] E. boschungi (Hubbs andTraut- E. inscriptum Jordan andGil- Ozarka Etheostoma

species group E. blennioides (Raney)], and attaches its (Hubbs and E. rupestre Gilbert and E. sellare Kirtland with Jordan and (Jor- (Jor- are 281 E. W. E. E. E.

282 ILLINOIS NATURAL HISTORY SURVEY BULLETIN Vol. 33, Art. 3 the species from extinction. Suitable spawning sites may be a limiting factor for the only extant population of E. sellare Clumping A Egg clumping was first reported in 1939 for E. maculatum Kirtland (Raney & Lachner 1939) but was unreported for other darters until observed in 1981 in E. aquali Williams and Etnier and E. microlepidum Raney and Zorach (Page et al. 1982). In preparation for spawning, the male selects a cavity under a large rock as a territory and future nesting site. Ultimately, a fe- male swims into the cavity being guarded by the male, wedges herself into the interface between the stone and the gravel substrate beneath the stone, and deposits eggs. As she does so, they are fertilized by the male. After spawning, the female leaves, and the male remains to guard the clump of eggs (Fig. 8). The adhesive eggs adhere to both the nest stone and the under- lying substrate material; if a stone is Fig. 8. — Egg-clumping behavior. (A) The male establishes a territory centered under a lifted from the water, a clump of adhe- large stone. (B) The female enters the territory sive eggs remains attached to it (Fig. 9). and wedges herself between the stone and the Egg clumping is known only among underlying substrate. (C) The male positions species of the subgenus Nothonotus of himself next to the female and fertilizes eggs as they are released by the female. (D) The male Etheostoma. remains to guard the clump of eggs.

Clumpers With 14 described and 1 undescribed species, the subgenus Nothonotus is one Etheostoma (Nothonotus) maculatum of the two largest subgenera of darters, (Raney & Lachner 1939) and intrasubgeneric relationships are E. (N) aquali (Page et al. 1982) unclear. The egg-clumping species are E. (N) microlepidum (Page et al. 1982) members of the E. maculatum lineage within the subgenus (Fig. 10), but it is Egg clumping is almost certainly a unknown at present at what point on direct derivative of the egg-burying be- the lineage egg clumping arose. E. havior (Page et al. 1982) characteristic rufilineatum has been observed to bury of other species of Nothonotus [known its eggs (Stiles 1972), and although in E. juliae Meek, E. rufilineatum spawning was not observed, Bryant (Cope), E. camurum (Cope), and E. tip- (1979) felt confident that E. acuticeps pecanoe Jordan and Evermann]. The Bailey also buries its eggs. Spawning transition from burying in some spe- behavior data on E. rubrum Raney and cies of Nothonotus to clumping in others Suttkus and E. moorei Raney and requires only that the male establish Suttkus should pinpoint the origin of a territory beneath a stone and that a egg clumping in Nothonotus. female deposit her eggs in the interface Although Etheostoma sanguifluum area between the stone and the under- (Cope) has been considered a subspecies lying substrate. of E. maculatum Kirtland by some September 1985 125 YEARS OF BIOLOGICAL RESEARCH 283

Fig. 9. — A male Etheostoma microlepidum and his clump of eggs on the underside of a stone removed from East Fork Stones River, Rutherford County, , on 6 May 1981. The male was guarding the eggs prior to their removal from the stream.

authors (Zorach & Raney 1967; Wil- additional 15 species in the subgenera liams & Etnier 1978), the distinctive Boleosoma and Catmotus of Etheostoma pigmentation of the first listed below. (especially the bright red spots at the The male of an egg-clustering spe- front and rear of the fin) of the male of cies establishes a territory centered E. sanguifluum is shared with E. about the cavity under a large (usually aquali Williams and Etnier but is ab- flat) stone. The cavity and the under- sent in all other species of the sub- side of the stone are cleared of silt and genus Nothonotus. Recognition of a debris by fin-wagging activities of the closer relationship between E. sangui- male. A ripe female enters the cavity fluum and E. aquali, than of either and, following courting by the male, taxon to E. maculatum (Fig. 10), re- rolls to one side and, once inverted, quires the elevation of E. sanguifluum rises and lays eggs on the underside of to specific status. The form heretofore the stone. The male inverts and ferti- known as E. maculatum vulneratum lizes the eggs, which are arranged by (Cope) also possesses the distinctive the female in a single-layer cluster (i.e., dorsal fin pigmentation and should be eggs are rarely laid on top of one named E. sanguifluum vulneratum another) on the stone. The female (Cope). leaves; other females sequentially may add eggs to the nest. The male remains and guards the eggs to hatching (Fig. Clustering 11). In species of Boleosoma, a log may The first report of egg-clustering be substituted for a stone. behavior in darters was by Seal in 1892 Egg clustering is similar to egg in a report on E. olmstedi Storer. Since clumping in that eggs are amassed then it has been documented in an under a stone and guarded by the male. 284 ILLINOIS NATURAL HISTORY SURVEY BULLETIN Vol. 33, Art. 3

4—P

0 rufilineatum sanguifluum microlepidum

LtJ UJ LLI LLI LLI LU

Fig. 10. - Hypothesized phylo- genetic relationships among some of the species of Nothonotus. Synapo- morph ies (black rectangles) are (1) dorsal fin with two red spots at the front, one red spot at the rear, (2) haloed red spots on the side of the male, (A) egg- clumping behavior, (3) black spots on fins of the female, and (4) red spots on the side of the body. Synapomorphous Character states were identified by outgroup com- parisons to Etheostoma ( Nothon- otus) tippecano E. (N)julia and E. (N) acuticeps.

It is dissimilar, and appears to be posed areas of rocks probably exposes "perfected:' in that every egg is exposed them to fewer predators although some and can be tended to individually by potential predators, e.g., crayfishes and the guarding male (Fig. 12). caddisflies (Brigham et al. 1982:9.6), The derivation of egg clustering are common under rocks. Once the from darters which attach their eggs to eggs under the stone are guarded by stones requires only that (1) eggs are the male, the survival rate undoubted- laid on the underside rather than the ly increases dramatically, and such a tops and sides of rocks, (2) eggs are concentration of eggs is quickly selected clustered in close proximity to one for. another rather than distributed over a Variation in behavior divides egg- broad area, and (3) the male remains clustering species into three groups: and guards the eggs. Laying eggs on (A) those in which both male and fe- the underside rather than on more ex- male invert only long enough to lay

September 1985 125 YEARS OF BIOLOGICAL RESEARCH 285

Clusterers Group A. Female and male briefly invert E. (Catonotus) squamiceps (Page 1974) E. (C.) olivaceum (Page 1980) E. (C.) neopterum (Page & Mayden A 1979)a Group B. Female only has prolonged inversion E. (C.) flabellare (Winn 1958)

, E. (C.) sp. = Duskytail (Etnier personal communication)a E. (C.) kennicotti (Page 1975a) E. (C.) obeyense (Page et al. 1981)a E. (C.) virgatum (Kornman 1980)a E. (C.) smithi (Page & Burr 1976) E. (C.) striatulum (Page 1980)a E. (C.) barbouri (Page et al. 1982)a Group C. Female and male have pro- longed inversions E. (Boleosoma) olmstedi (Atz 1940) E. (R) nigrum (Winn 1958)a E. (R) podostemone (Jenkins 1980)a E. (R) perlongum (Lindquist et al. 1981) E. (B.) longimanum (Page et al 1981)a

Fig. 11. — Egg-clustering behavior. (A) The a male establishes a territory centered under a Although known to be a clusterer, large stone. (B) The female enters the territory group assignment is predicted from and selects a site for egg deposition on the under- the behavior of closest relatives and side of the stone. (C) The female inverts, rises, is not based on actual observations. and deposits eggs on the stone; as she does so, the male follows and fertilizes the eggs. (D) The male remains to guard the cluster of eggs. The phylogenetic sequence of breed- ing behaviors among Catonotus is con- and fertilize each release of eggs cordant with a phylogeny of the (usually 1-5 eggs); (B) those in which subgenus based on morphology in that the female, once inverted, remains in- three synapomorphies unite the E. verted for a prolonged period of egg lay- flabellare Rafinesque lineage as ad- ing (several minutes to a few hours) but vanced and apart from the E. squami- the male only briefly (a few seconds) ceps Jordan species group (Fig. 13). and periodically inverts; and (C) those Both Catonotus and Boleosoma must in which both male and female remain have evolved from egg-attaching pre- inverted for an extended period. Ob- cursors. Although egg clustering itself viously, group B represents an advance- could be considered a synapomorphy ment over group A, and group C rep- uniting these two subgenera, they dif- resents an advancement over group B. fer markedly in their morphology and Group A includes the primitive species do not appear to be sister groups (Page of the subgenus Catonotus; B, the ad- 1981). Boleosoma shares derived char- vanced species of Catonotus (Page acteristics with other groups of Ethe- 1975b); and group C, species of the °stoma (Fig. 14) and almost certainly subgenus Boleosoma. Winn (1958) had an origin independent from that of distinguished between behavior types Catonotus. It appears to be most closely B and C. related to K (Ioa) vitreum (Cope), an 286 ILLINOIS NATURAL HISTORY SURVEY BULLETIN Vol. 33, Art. 3 egg-attaching species. The sister-group EVOLUTION OF PERCID of Catonotus should first be sought SPAWNING BEHAVIORS among egg-attaching species; however, if the attaching precursor now is ex- tinct, an egg-burying group may be the Combining the evolutionary sequen- closest extant relative. ces discussed above produces the phyl-

Fig. 12. — Male Etheostoma neopterum and his cluster of eggs on the underside of a stone removed from Birdsong Creek, Benton County, Tennessee, on 15 April 1978. The male was guarding the eggs prior to their removal from the stream. September 1985 125 YEARS OF BIOLOGICAL RESEARCH 287

Fig. 13. — Hypothesized phylogenetic relationships among species of Catonotus. Synapomorphies (black rectangles) are (1) four infraorbital pores, (2) maximum standard length less than 50 mm, (3) bar pattern on the cheek, (4) blue-edged red fins on the breeding male, (5) large gold knobs on the first dorsal fin, (6) nape unscaled, (7) prepectoral area unscaled, (8) infraorbital canal widely interrupted, (A) type B clustering behavior (the female remains inverted during spawning), (9) infraorbital canal narrowly interrupted, (10) caudal peduncle with three black spots, (11) broad, flat nonbifurcate genital papilla on the female, (B) egg-clustering behavior. Synapomorphous character states were identified by outgroup comparisons to Etheostoma (Psychromaster) tuscumbia and E. (Fuscatelum) paruipinne. ogeny depicted in Fig. 15. There appear group of Catonotus); rather, all alpha to be no reasonable alternatives to any and beta precursors of Boleosoma are of the transitions depicted. However, extinct. each type of behavior could have arisen, The phylogeny (Fig. 15) supports and in some instances almost certainly the contention that darters, the most did arise, more than once. For example, primitive of which are buriers, are although gamma clustering results derivatives, and probably the sister from a modification of beta clustering, group, of Stizostedion. This position it does not mean that the only extant disagrees with the conclusions of Col- gamma-clustering group of darters lette (1963) based on osteology, but it (Boleosoma) arose from the only extant agrees with those of Hubbs (1971) based beta-clustering group (i.e., the flabellare on the survival of intergroup percid

288 ILLINOIS NATURAL HISTORY SURVEY BULLETIN Vol. 33, Art. 3 hybrids. A PHYLOGENETIC classification Each step in the evolution of spawn- necessitates the recognition of the sub- ing behaviors represents, for the spe- families ETHEOSTOMATINAE (containing cies in which it evolved, a survival the tribes LUCIOPERCINI, ETHEOSTOMATINI, advantage over its precursor. Pit broad- and ROMANICHTHYINI) and PERCINAE casting concentrates the eggs in an (Table 1). area subsequently guarded by the male

Doration VaIllantia Ioa Boleosoma E 0 E E E E = 0 --. O .-- 0 C A) a) = V) E 0 0) 0 0 0 0 0 0 E A), = E E --, IN S_ A.) 0 4- 0 -.-■ DL U) "--4 0 L- S- U) .--4 CH ..-., U) > 4-. 01 E L. C 4- a) -C) :E" ..--. ..--. a) 0

U) 0 (...) > = 0 A -, podostemone

Fig. 14. — Hypothesized phylogenetic relationships among species of the subgenera Boleosoma, loa, Vaillantia, and Doration. Synapomorphies (black rectangles) are (1) broad branchiostegal mem- brane connection, (2) red-orange spots on the breeding male, (3) elongated second dorsal fin on the breeding male, (4) overall dusky breeding male, (5) bifurcate genital papilla on the female, (6) white knobs on paired fins, (A) egg-clustering behavior, (B) eggs attached to rocks, (7) black bridle around the snout, (8) extremely short second dorsal fin, (9) spatulate genital papilla on the female, (C) egg- attaching behavior, (10) blue bars on the adult male, (11) blue and red bands in the first dorsal fin of the adult male, (12) brown-black x/w marks on the body. Synapomorphous character states were identified by outgroup comparisons to Etheostoma (Psychromaster) tuscumbia and E. (Litocara) nianguae. September 1985 125 YEARS OF BIOLOGICAL RESEARCH 289

- Clustering

13 - Clustering

a - Clustering

Fig. 15. — Hypothesized evolutionary relationships among percid breeding be- Attaching haviors. Clumping

Burying

pit-Broadcasting Stranding

open-Broadcasting and thus increases the probability of eggs under a partially elevated stone, their survival by reducing predation. thereby enhancing crypticity. The ad- Also, S. lucioperca males fan the eggs, vantage of male egg guarding followed. presumably to prevent them from be- The derivation of attaching from ing covered by silt, and thereby reduce burying (or from any other behavior) is mortality due to anoxia. difficult to envision. However, the Burying eggs reduces exposure to presence of both behaviors within predators and probably to parasites, several (at least three) subgenera of enhancing survivability. However, eggs Etheostoma leaves no doubt that one is can be buried only in flowing water derived directly from the other. The , usually in gravel but some- strong positive correlation between times in sand, where burying does not primitive morphology and burying subject the eggs to especially low oxy- (e.g., all species of Percina are buriers) gen levels such as would occur if eggs and between advanced morphology and were buried in slow-flowing or standing attaching (e.g., in the subgenus water. Buriers are constrained behav- Boleichthys) clearly indicates that the iorally to flowing water and coarse direction is from burying to attaching. substrates. Consequently, stream mod- For darters living in slow-flowing or ifications, such as impoundments and standing water (e.g., Boleichthys species), channelization, prevent successful the advantage of attaching is obvious; spawning by these species. with demersal and adhesive eggs, the In the primitive state, species of only alternatives to attaching are bury- Nothonotus bury their eggs in the sand- ing eggs in an oxygen-poor substrate gravel mixture on the downstream side (often rotting vegetation and mud) or of a large stone in fast water. Clump- migrating to suitable habitats for bury- ing, as discussed above, evolved in a ing. Similarly, species living in bedrock species of Nothonotus which buried its pools [e.g., E. simoterum (Cope)] where 294 ILLINOIS NATURAL HISTORY SURVEY BULLETIN Vol. 33, Art. 3

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