Anim. Behav., 1987, 35, 1145-1 I58

Paternal defence, cannibalism and polygamy: factors influencing the reproductive success of painted greenling (Pisces, Hexagrammidae)

E D W A R D E. D EMA R TI N I

Marine Science Institute, University of California, Santa Barbara, California 93106, U.S.A.

Abstract. The relative costs and benefits of paternal egg-guarding behaviour were identified for painted greenling, Oxylebius pictus, a small fish inhabiting temperate rock reefs. Because males must guard embryos against conspecifics of both sexes and against other fishes, their movements were curtailed, and an energy cost resulted. The males' somatic condition declined in proportion to the time spent guarding. Paternal males partially compensated by cannibalizing a small fraction of their progeny. Male O. pictus thus parasitize females by consuming their spawn. Polygamous matings were nonetheless advantageous for individual females as well as for males. The reproductive success of males and females increased for male broods with greater numbers of clutches, because there was a general dilution of predation loss in larger broods. The success of females, moreover, varied depending on the rank (chronological) order of spawning; success was greater for those that contributed earliest to the male's brood. The results support the hypothesis that the breeding cycles typical of paternal teleosts have evolved partly because of energy costs imposed by site-dependent care. For multiple-clutch species with protracted breeding seasons like O. pictus, the long-term benefits of polygamous spawnings perhaps outweigh short-term losses sufficiently for filial cannibalism to evolve and be maintained. Alternatively (or in addition), the foraging milieu may exert a stronger average environmental influence than kin selection does.

Classical evolutionary theory has characterized the relations between mates as cooperative ventures that benefit all partners and their populations. Trivers (1972), Alexander (1974) and others, how- ever, have theorized that cooperation may not be the norm, or even expected in most cases. The stable resolution may be less than ideal for either s e x .

The options confronting females regarding the choice of unmated versus already mated males, or confronting males regarding paternal care versus continued matings with additional females, typi- cally generate a conflict between the sexes (Down- hower & Armitage 1971; Trivers 1972; Davies & Halliday 1977; Emlen & Oring 1977; Parker 1983).

Polygamous mating systems, in particular, generate conflict between the sexes (Trivers 1972; Alexander 1974; Emlen & Oring 1977). Polygynous systems involving lone paternal care of demersal embryos are especially prevalent among teleost fishes (Blumer 1979), and have generated much recent debate over evolutionary origins and current adaptations (e.g. see Gross & Sargent 1985, and references therein). Males obviously benefit from polygyny. But are teleost breeding systems with paternal care necessarily cases where only males

(Emlen & Oring 1977), and not females, benefit from territorial defence of embryos and polygyny (Turner 1985)?

In this paper, I first summarize the mating system of the painted greenling Oxylebius pictus. I then discuss the nature, function and ecological implica- tions of male parental care and test a series of predictions involving the cannibalistic behaviour of males. Data on the mating and reproductive success of individual males and females follow. I use individual fitness parameters to assess the adaptive trade-offs (costs and benefits) of poly- gamy. I conclude with a comment on male breeding cycles in teleost fishes.

Reproductive Biology and Mating System

The painted greenling is a small (to 100 g), territorial, hexagrammid fish that is abundant, conspicuous and dimorphic in colour and beha- viour (DeMartini 1985). Males are smaller and have shorter lifespans than females; adult sex ratios are about one male to two females (DeMartini & Anderson 1980).

Adult O. pictus, presumably unrelated, spend most of their solitary lives within small areas (less

1145

1146 Animal Behaviour, 35, 4

than 10 m 2) of reefs, whereupon larvae recruit after a lengthy (1-3 month) planktonic dispersal stage. The larvae originate from walnut-shaped clutches of eggs that are spawned in an area less than 100 cm 2 among invertebrate encrustations at a central site within the male's territory. The embryos are tended by the male until hatching (approximately 2-5-3.5 weeks, depending on the temperature), but there is no care of larvae after hatching. Fecundity is positively related to the size of the female, and, in Puget Sound, Washington, U.S.A. (47" 40' N, 122 ~ 30'W), females produce three clutches, each con- taining 1500 5000 eggs, per 3-month breeding season (DeMartini & Anderson 1980).

On most Puget Sound reefs, adults occur at high densities of about 0.3 per m 2, and the males' territories cover about 2 m 2 (DeMartini & Ander- son 1980; DeMartini 1985). Adult males forage by searching the sessile epibiota within their home ranges for small crabs, shrimps and other crusta- ceans. The males' territories are generally conti- guous and packed into central, high-relief areas (DeMartini & Anderson 1980). Juveniles and females occupy outlying areas (DeMartini 1985). Successful (larger, older) males acquire and tend broods that contain the clutches of one or more females during each of several consecutive breeding cycles (van Iersel 1953). Each month-long breeding cycle consists of a 10-day mating phase and a 20- day parental phase (van den Assem 1967). Females desert the male and eggs after spawning. Indi- viduals of each sex have more than one mate (DeMartini 1985) and there is no pair bond, but this does not imply an absence of selectivity.

Predictions

I tested the following predictions and specific hypotheses. (1) Paternal males provide necessary protection, but other tending functions are non- essential; (2) tending males incur energy costs because of site-restricted foraging; (3) a male's costs while tending are partly compensated by filial cannibalism (Rohwer 1978) of a small fraction of the embryos tended; and (4) polygamy benefits both sexes, but paternal filial cannibalism has generated a suite of differing male and female mating strategies that partly compromise the reproductive success of individuals.

Regarding prediction 1, if orphaned spawns could survive as well as male-tended ones, the

hypothesized protective function of paternal care could be rejected. Conversely, if unprotected spawns perished, but protected (caged) ones sur- vived, then tending males must provide protection rather than simple, sanitary brood care.

Regarding prediction 2, tending spawns at a central site within the territory might restrict a male's foraging movements and food intake. Pater- nal males should remain closer to the centre of their territories while tending and have less opportunity to forage. The energy cost resulting from restricted foraging opportunity should be proportional to the amount of time spent tending spawns.

Regarding prediction 3, males should canniba- lize more than females in species of territorial male- tenders in which raiding females do not school to overwhelm males (Kynard 1978; Rohwer 1978; Dominey & Blumer 1984). Moreover, parental and non-parental males should differ in their extent of cannibalism. Since paternals should only partially consume tended clutches but non-paternal raiders should steal as many embryos as possible (Rohwer 1978), non-paternals should consume as many embryos, or more, than non-raiding filial canni- bals.

The likelihood of filial cannibalism should also vary throughout breeding cycles and breeding seasons (DeMartini 1976; Rohwer 1978; Dominey & Blumer 1984). Males should cannibalize off- spring near the end of breeding cycles, when they are hungrier. But since older embryos are more likely to survive to hatch, mature and reproduce, males should selectively cannibalize the most recently laid (Rohwer 1978) among the pigmented embryos present (whose advanced age may be visually assessable by females). Conversely, if raid- ing were the major source of embryo cannibalism by paternal males, most ingested embryos should be in a n early stage of development, since raids should be more successful against neighbours that are still in the mating phase and therefore less diligent guardians (Pressley 1981). Paternals should frequently consume large numbers of pig- mented embryos only if most of their embryo- eating is filial cannibalism.

Female O. pictus should avoid spawning with males that have entered the parental phase of the breeding cycle and thus are more apt to cannibalize their own young. If so, males should sometimes cannibalize entire single, pigmented-development clutches if expected mating success is greater than

DeMartini: Mating system of painted greenling 1147

or equal to two females (Rohwer 1978). Hence, entire single clutches should be more frequently lost than first clutches in multiple-clutch broods.

Regarding prediction 4, males obviously benefit from polygyny, but individual females might also benefit if the expected hatching success of male- tended clutches increased in broods comprising greater numbers of clutches. A major hypothesis I tested was whether mating success positively influenced the reproductive success of females as well as males (see Loiselle & Barlow 1978; Blumer 1979), and if so, whether or not the relation was linear and independent of the rank (chronological) order of clutch contribution to the brood.

M E T H O D S

Paternal Care

To evaluate the potential protective and brood- ing functions of paternal care, I orphaned clutches of embryos by removing tending males. Some of these clutches were protected from predators with 10 em 2 hardware cloth enclosures with meshes of 0.3 and 0-6 cm; other orphaned spawns were left unprotected. Male-tended spawns served as con- trols. The protective function of paternal care was also inferred from field observations of the relative frequency of aggression displayed by tending and non-tending males towards various classes of con- specifics and other potential predators of embryos.

Male Foraging Restriction

Males were individually tagged on two reefs (Rock, Point) in Puget Sound during 1973 1974 (DeMartini & Anderson 1980; DeMartini 1985). When first seen on each subsequent dive, each tagged male's position was noted with respect to the distance from its central site, and the male's tending status was recorded. Because of potential differences in home range size and propensity to leave the central site, each male was used as its own control in a paired-comparison test, with males as replicates.

I estimated changes in somatic (gonad-flee) weight for males of various reproductive histories at the Rock and Point reefs in 1973. Tagged males were hand-netted at the beginning and end of the 1973 breeding season; their body lengths were determined (with an accuracy of + 1 mm; DeMar-

tini 1985), and an index of somatic condition (flank breadth) was measured in situ with vernier calipers (accuracy + 1 mm). Somatic wet weight was estimated from flank breadth, using total length as a covariate, based on data for male greenling collected at the Seattle reef (DeMartini & Ander- son 1980) during the summer of 1974. The extent of paternal tending was determined for Rock and Point males based on a census of each male and its spawning sites, repeated at intervals of 2~4 days throughout the breeding season.

Filial Cannibalism of Embryos

The natural incidence and extent of embryo cannibalism was characterized, in part, based on 13 collections of adult males and females made at weekly to fortnightly intervals throughout the 1974 breeding season. Fish were speared from areas at the Seattle reef that were undisturbed prior to the experiment (DeMartini & Anderson 1980). On each sampling date 3-21 (mean = 10) fish of a range of sizes of each sex were randomly collected. Whenever possible, males were scored as paternal or non-paternal at the time of collection; tended embryos were also collected. These data were supplemented by collections of males speared from non-monitored areas of the Rock and Point reefs during 1973, 1974 and 1975. Data were grouped by collection date for analysis.

Stomach contents of males and females were quantified using a prey contents index (PREYINDX) based on the relation, PREYINDX=(weight of prey/weight of fish) times a constant. The constant (103) was used to adjust all values greater than 1.0. The index was calculated for fish of all body sizes pooled, since there was no relation (both P > 0'1) between total stomach contents weight and body weight for adult sample fish of either sex. Somatic wet weight of fish was determined to the nearest g, and wet weight of total stomach contents to 0.1 g. Stomach contents were classified as conspecific embryos and other prey, and their relative contribution was estimated by percentage volume (Hellawell & Abel 1971). Embryos were classified as early stage (unpig- mented development) and later stage (pigmented development). The fertilized eggs (approximately 1.4 mm in diameter) of O. pictus were distinguished from eggs of other fishes by their size and the unique presence of a single, large (200-300 #m), amber-coloured oil globule.

1148 Animal Behaviour, 35, 4

Filial cannibalism was most strongly inferred from developmental similarities between ingested and tended embryos. Breeding cycles of females and males are asynchronous, however. At most instances during the breeding season on a particu- lar reef, various males are tending clutches that range in age from just fertilized to near hatching. Neighbouring males may guard embryos having the same developmental stage as a filial cannibalis- tic male. Hence, embryos present in the stomach of a cannibalistic guardian that resemble those guarded by the male do not provide firm evidence of flial cannibalism. To counter these chance overlaps, I estimated an index of overlap as INDOVER = PSg,i/PSg,g, where PSg,i = percentage similarity between embryos cannibalized and guarded by a male, and PSg,g=percentage simi- larity between embryos guarded by a paternal male and guarded by a randomly chosen, near-neigh- bouring male. I interpreted greater overlap in similarity than expected from breeding synchrony as evidence of filial cannibalism.

Mating and Reproductive Success of Individuals

Totals of 350 and 85 field-hours (during its breeding and non-breeding seasons, respectively) were spent observing the social and related beha- viour of O. pictus over 4 years (1972-1975) as part of a complementary study (DeMartini 1985). Observations were made at eight natural and artificial reef sites in Puget Sound, using scuba at depths of 5-15 m. Seventy-five per cent of the total observation time was spent at the Rock and Point reefs during 1973 and 1974.

To determine the mating success and reproduc- tive success of individuals, I tagged 45 adult males at the Rock and Point reefs and subsequently monitored their reproductive status during one or both breeding seasons. I tracked 38 males through the end of the 1974 season. Forty-three were tagged

p r i o r to the 1973 study; seven males disappeared, and two males recruited to the Point breeding population in 1974. Tagged fish consisted of all of the territorial males present within a large, repre- sentative area at each of the two reefs.

The mating success of individual males, here defined as the number of clutches acquired (number of females spawned with), was estimated based on the cumulative number of different clutches observed on a point census of each male and its spawning site, repeated at intervals of 2 4

days throughout each breeding season. Individual clutches were easily recognizable because of their discrete nature and unique combinations of size, yolk coloration, shape and position. Clutches within broods were mapped on plastic slates with respect to adjacent invertebrate encrustations. In this manner I could estimate the spawning dates of the clutches in each brood and follow the fate of each clutch over time.

I estimated male reproductive success, defined as the number of larvae successfully hatched, based on the percentage of each clutch (female reproduc- tive success) that was seen hatching or that survived past 80% time to hatching. (This time was 15 18 days, at water temperatures of 10-13~ Percent- age hatch was estimated (__ 5%) based on changes in the outline of individual clutches evaluated on successive visits. Percentage hatch was an accurate measure of the absolute number of larvae hatched because the number of embryos present in an intact clutch did not vary with the number of clutches in the brood (Kruskal-Wallis H = 3.6, dr= 2, N = 90 broods, P > 0"1). Size of clutch also did not vary with spawning order of the clutch within broods of a specific number of clutches (H=4.4, dr=5, N= 90, P > 0.3) or all numbers of clutches pooled (H=2.4, df=2, N=90, P=0.3).

RESULTS

Nature and Function of Paternal Care

]~mbryo care by male O. pictus consists of guarding embryos against conspecifics and other predators (Table I). Major heterospecific predators are several species of small sculpins, Artedius spp., which hide in crevices within and outside of male greenling territories, and a relatively large-bodied, but small-mouthed, invertebrate-feeding surf- perch, Embiotoca lateralis, Non-guardian males primarily attack other males. Guardian males direct most defence against conspecific males, but also attack other species (Table I). Most heterospe- cific defence is directed at egg-eaters, regardless of whether the species shares O. pictus' foraging or sheltering guilds (Table I). Defence is primarily passive: predators are usually deterred by the male's physical presence. I observed no fanning or other sanitary behaviour such as weeding out unfertilized eggs or dead embryos (occasionally present in low numbers within clutches).

DeMartini: Mating system o f painted greenling 1149

Table I. Number of aggressive acts (observed in 382- I h) by O. pictus during the 1972-t975 breeding seasons on eight Puget Sound Reefs

Mating status of aggressor male*

Identity Non- of aggressee Paternal paternal Unknown

Adult male O. pictus 53 59 48

Adult female O. pictus 18 34 17

Artedius spp.t~: 16 I 0 Embiotoca

lateralistJ; 13 3 0 Sebastes

auriculatus~ J;w 4 0 0 Sebastes

eaurinus~f J;w 3 0 0 Sebastes

maliger'~w 2 1 0 Damaliehthys

vacca~ 3 0 0 Chirolophis

nugatorY( 2 0 0 Hexagrammos

decagrammus?~ 1 0 0 Sebastes

emphaeus 1 0 0 Jordania

zonopet~ 0 0 0 Nautichthys

oeulat~?fasciatus~w 0 0 0 Cancer productus'~�82 2 0 0 Pugettia

produetar182 2 0 0

All conspecifics 71 93 65 All heterospecifics 49 5 0

* Adult female and juvenile O. pietus never attacked heterospecifics. An O. pictus (of undetermined sex) was only once seen attacking a heterospecific (E. tateralis) in over 147 h of observation during the non- breeding seasons of 1972-1974.

t Species in the same feeding guild as O. pictus (DeMar- tini 1976; Miller et al. 1980). Species of egg predator (DeMartini 1976, and refer- ences).

w Species that uses the same reef crevices as those occupied by O. pictus (E. DeMartini, personal obser- vation).

�82 Brachyuran crab.

test, P=0-005; Table IIa). Orphaned, but caged, embryos developed normally to hatching (P=0"004; Table IIb), and caged embryos never developed fungal infections despite lack of paternal care. If orphaned and left uncaged, however, embryos were consumed, most frequently by Arte- dius spp., within 15-30 min of the male being removed. On average, a slightly greater percentage (43-73%: see Table 3 in DeMartini & Anderson 1980) of embryos were guarded until hatching in the monitored populations than were successfully guarded during the experiments (Table IIa).

Male Foraging Restriction

Males generally occurred closer to their central sites while guarding embryos (J(_ SE = 53 __ 4 cm) than while not guarding (108 __ 7 cm; paired t-test: t=8.5, N=35 males, P<0.0001).

Paternal males at the Rock and Point reefs gained an average of about 1% in somatic weight during the 1973 breeding season, while growing 1-15% in length as an inverse function of initial length. Frequent guardians (males that spent greater than a median 45% of the 100-day breeding season tending embryos) barely maintained their weight (lost 0.2 + 0-7 g), whereas infrequent guar- dians (males that spent less than 45%) increased by more than 2% in somatic weight (gained 1.4 +_ 0.4 g). The hypothesized greater energy cost incurred by males that are frequent guardians is supported (approximate t-test: t '=1.95, N=31 males, P=0.03). Males that were frequent guardians averaged 56% (range 46-87%) of the season tend- ing embryos, whereas infrequent guardians aver- aged 24% (range 0-44%).

Estimated declines in somatic weight allowed for nominal differences in the mean (_ SE) body lengths and somatic weights of frequent (185_+ 2 ram, 64 _+ 2 g) and infrequent (183 _+ 2 mm, 63 _+ 2 g) guardian males in the sample populations. Somatic wet weight (in g) was related to flank breadth (FB, in ram) and to total body length (TL, in ram, as covariate) by the relation SOMAWT=10 .75- 0 .05TL- 2.70FB + 0-03(TL x FB), where r 2 = 0-97, N = 4 9 , P < 0-0001.

Paternal guarding of embryos is necessary and resulted in greater numbers of embryos hatched than if the embryos were not guarded (Fisher exact

Filial Cannibalism of Embryos

I saw only three instances of apparent raiding and two of filial cannibalism by males in over 500 h of scuba observations. While confirming the

1150 Animal Behaviour, 35, 4

Table II. Fates of uncaged and orphaned embryos

No. that survived No. that died

(a) Uncaged Orphaned* 0 14 Male-guarded (controls) 13 21

(b) Orphanedt Caged 7 0 Uncaged (controls) 0 15

* Embryos were orphaned by spear removal of guardian males at the Seattle, Rock and Point reefs during 1973-1975.

t All caged, orphaned embryos developed at a normal rate to hatching; all spawns that 'died' had disappeared within 7 days, probably because of predation, since embryos of early development were used in the tests.

na tura l existence of bo th filial and he te rocanniba- lism by males, direct observat ions were insufficient to quant i fy the two types of behaviour and infer- ences had to be based on indirect evidence.

The relative impor tance of raiding and filial cannibal i sm was inferred from the frequency and extent of male and female cannibal i sm of different developmental stages of embryos. Males on the Seattle reef cannibalized embryos more frequently 0f2= 60"0, df= 1, P<0"001) and to a greater aver- age extent than did females (ANOVA: F = 14.0, dr= 1, 232, P<0"001 ; Table III). The weight of embryos cannibalized, whether s tandardized to body weight or not, was unrelated to the canniba l ' s

body weight (bo th Spearman 's rank corre la t ion coefficient rs < 0" 1, N = 96 males, bo th P > 0.75) .

Pa terna l O. pictus, moreover , cannibal ized embryos more frequently than non-pa te rna ls ()~2 = 4-0, df= 1, P < 0.025; Table III). Paternals and non-pa te rna l s cannibal ized embryos to equivalent extents when they cannibal ized (ANOVA; F = 0.4, dr=l, 49, P = 0 - 5 5 ; Table Il l) . The high mean extent of embryo cannibal ism by bo th classes of males (approximately 50- t 50 embryos or 30-45% of the prey volume of male cannibals , Table I l l ) is equivalent to abou t 2 -6% of the average female's clutch, if all embryos were cannibal ized f rom a single clutch. Since a mean of 1 '2 (_+ 0"05) different

Table Ill. Contents indices (PREYINDX), average number of embryos cannibalized, and frequency of cannibalism by adult O. pictus

Mean PREY1NDX (4-SE)*

Average no. Frequency of embryo embryos cannibalism

per stomacht (embryo stages)

Other All prey Embryos prey

No. Early Late All % No. fish Mean Median stage stage stages cannibals fish

All females~. 5.8+0.6 0"8_+0"6 6.5+0.9 118 141 16 23 6 30 25 120 All malesi~ 4.8_+0-6 3-2_+ 1.0 8.0_+ 1.3 128 155 48 59 47 96 75 I28 Non-paternalmales 7-1_+2.5 4-8_+6-8 1i-9_+_5-9 33 246 80 9 18 23 70 33 Paternal males 6.4 _+ 2.8 2-7 4- 1.5 9.0 4- 3.2 22 90 34 14 9 21 95 22 Paternal malesw 5.7 _+ 1-5 4-5 -+ 2.0 10.2 _+ 2.6 42 82 50 30 29 42 98 43 Mating phase 6.2 4- 1-7 4-5 4- 2-8 10.7 4- 2.7 24 182 48 20 9 23 96 24 Parental phase 5.1 4- 1.4 4-4 4- 2.5 9'5 4- 2.9 18 187 35 10 20 19 100 19

* Including cannibals and non-cannibals; weighted means and sEs based on 13 and five dates for the general sex and male tending categories, respectively, and based on 10 dates for male mating-phase categories.

-~ For stomachs containing cannibalized embryos. :~ Sample fish from the Seattle population, April-August 1974. w Includes 20 additional paternal males collected from the Rock and Point populations in August 1973, August 1974

and June 1975.

DeMartini: Mating system of painted greenling 1151

embryonic stages occurred per male cannibal's stomach, the actual value was less than 6% of an average clutch per stomach. The gut evacuation. rate of O. pietus is unknown; however, a reasonable (2-day) interval between emptyings would equate to less than 3% of a clutch per stomach per day.

Pigmented-stage embryos were cannibalized more frequently by paternal-phase than by mating- phase guardians (~2 .~_ 6' 1, df= 1, P < 0"01). Females cannibalized more early and fewer late-develop- ment embryos than did male cannibals (X2=4.4, df= 1, P<0.025).

Total loss of single clutches (81% of 53 broods) occurred more often than total loss of first clutches in 37 two-clutch broods (49%) or in 87 broods of three or more clutches (21%; Z2=49.0, df=2, P<0.001).

Last, the overlap in similarity of development between 128 stages of embryos tended and eaten by 37 paternal males (PSg,i = 0.46, SE = 0.10) averaged more than twice the overlap between the embryos present in 157 clutches guarded by these males plus their near-neighbours (PSg.g = 0"20, SE = 0.10; Z2=21'5, df= 1, P < 0.001). White embryos (dead when ingested) occurred in only 8% of all male cannibals' stomachs.

Mating and Reproductive Success

Male mating success was 0~10 clutches per breeding cycle, and 0-22 clutches per breeding season at the Rock and Point reefs during 1973 and 1974. Males averaged 7'5 clutches per season for the three potential brood cycles. Males that acquired eggs spawned with 3.5 females per cycle during an average 2.3 brood cycles per season.

Male reproductive success varied as a positive function of mating success. Males that spawned with two females successfully guarded a greater fraction of both clutches than did males that spawned with one female (Fig. 1). Male reproduc- tive success, in fact, increased monotonically with additional matings (Spearman's rank correlation coefficient r~=0.781, N= 184 broods, P < 0.01; Fig. 1).

Female reproductive success, or the average percentage hatching success per clutch, also increased with male broods containing greater numbers of clutches (r~=0'423, P<0'01; Fig. 1). On average, female success was about one-half of male reproductive success (Table IV). An apparent asymptote in mean success in the largest broods

c=

E = =

I

100

80 :_=

g

60 ~=

g 40 "~

20

i lO

Number of clutches in brood

Figure l. Mean number of clutches hatched (total eggs) and mean percentage hatching success per clutch in male broods of different numbers of clutches. Data are the average reproductive success of 38 tagged males and the females that spawned with them, at the Rock and Point reefs during 1973 1974. Sample sizes are numbers of male broods. Vertical lines represent 2 sE.

suggests a diminishing average advantage to females spawning with highly polygynous males (Fig. 1).

The interrelations of female reproductive success and the mating and reproductive success of males was indistinguishable among the 4 population- years (r~ all P>0-05). Average male mating and reproductive success, though, varied within a sea- son and between years at each reef. The mating success of tagged males averaged 51% greater at the Rock reef, and 13% greater at the Point reef in the second year. Tagged males, of course, grew and gained mating success between 1973 and 1974 (signed-ranks test, z=2"18, N=28 males, P=0"015), but relative success among males remained consistent over the 2 years (r~=0.51, N=31 males, P<0-01; Fig. 2). Mean hatching success was greater during 1973 and during the first and second thirds of the breeding season (Table V).

1152 Animal Behaviour, 35, 4

Table IV. Estimated means and variances of reproductive success and intensity of sexual selection (Is)* for individual males and females

Male success Female success (no. clutches) (no. clutches)

Population-year Mean Variance? /s Mean Variance~ L

Rock reef, 1973 3.2 4.2 0.41 1.6 0.9 0.35 Rock reef, 1974 2.8 5.2 0.66 1.2 0.5 0.35 Point reef, 1973 6.2 19.6 0.51 2.0 0.6 0.15 Point reef, 1974 4.5 14.9 0.74 1.3 0.7 0.41

* L= Variances/(Means) 2 (Wade & Arnold 1980). ? Mean and variance of male success based on the cumulative fraction of

clutches hatched out of all clutches acquired by each male during each population-year. Mean and variance of female success based on the mean fractional hatch per clutch averaged over all male broods monitored each population-year, with means weighted by a factor of three (because females spawn three times each breeding season) and with variances weighted by nine (three-squared).

, 1 ~ 1 , I = l l l ~ l , 6 , 1 , 1 , 1 1 1

20

i , , ,~ - o

-~ - - O

~ r ~ 12 = x . ~ o

8

-~ ~o r

~ " 4 .=,,.=,~ �9 0

Dv~[I ~ I , I , I i I i I n I a I ~ I 4 8 12 16 20

No. clutches per male-season (1973)

Figure 2. Observed mating success of individually tagged males at the Rock (closed circles) and Point (open circles) reefs in 1973, plotted against success of the same male in 1974. Diagonal line is added to indicate null hypothesis of no difference between years. Small arrow indicates the only male that changed spawning site between 1973 and 1974.

Data on hatching success of clutches for the 4 population-years pooled show some intriguing relations to the rank order of clutch contributions. On average, the expected reproductive success of females, although greater for later spawnings in larger broods (Spearman's rank correlation coeffi- cient rs=0"90, N = 5 rankings, p<0-05 ; Fig. 3),

declined for later spawnings within a given brood size (Fig. 4). Hatching success was higher for given rank-laid clutches in progressively larger, multiple- clutch broods (i.e. second rank-laid clutch: Krus- kal-Wallis H = 8.6, df= 3, N = 118, P < 0.05; third rank-laid clutch: H = 8 . 4 , df=2, N = 7 1 , P<0-025; fourth rank-laid clutch: H = 4 . 3 , df=l, N = 3 3 , P < 0.05; Fig. 4). The success of later-laid clutches declined at similar rates in broods of two, three or four clutches; a lesser rate of decline was evident in broods of five-six clutches (Fig. 4). The mean hatching success of first-laid clutches was progres- sively greater in larger broods, and was least in single-clutch broods (H=55 .8 , df=4, N=167 , P<0 .001; Fig. 4).

Rate of acquisition of clutches also varied signifi- cantly with the sequence and number of clutches present. Latency decreased between later rank spawnings. Males acquired second clutches faster (on average after 3.5 + 0-7 (SE) days, N = 66 cases) than they acquired their first clutch (6"0 ___ 0"4 days, N = 65), and they acquired a third even slightly faster (2 .7+0 .5 days, N = 3 9 ; sign-tests, both P<0-001).

The variance in reproductive success of indi- vidual male O. pictus was only about 0" 5-1-3 orders of magnitude larger than the variance in female success. These estimates of reproductive success would accurately reflect ma l~ fema le differences in intensity of sexual selection, if females choose males independently of whether, and to what

DeMartini: Mating system of painted greenling 1153

Table V. Mean percentage hatching success per brood during the 1973 and 1974 breeding seasons

Percentage hatch by period within breeding season*

Early Middle Late Population-year (May-June) (June-July) (July August)

Rock reef, t973 54 _+ 15(9) 54 _+ 13(12) 48 + 28(4) Rock reef, 1974 31 _+ 9(14) 47 • 10(15) 44 • 15(6) Point reef, 1973 72 +_ 6(19) 70 • 6(19) 57 • 12(9) Point reef, 1974 33 • 8(20) 54 _+ 7(21) 44 _+ 8(15)

* Standard errors and sample sizes (number of male broods) are noted.

E

J= g

80

75

7oJ

50

All brood sizes pooled

1 2 3 4 5 Rank order in which clutch was laid

Figure 3. Mean percentage hatching success of clutches of different rank order of spawning in broods of all numbers of clutches pooled. Data reflect the average reproductive success of hypothetical females that chose to spawn independently of whether males were unspawned, mono- gamous or already polygynous. Sample sizes are number of clutches (all brood sizes pooled). Vertical lines are • 2 S E .

9 0

..= 8O

~ 7 0

6o

== ' - 50

~40

~. 30

20

10

I J I 1

Various brood sizes

~2L._.20

22 0 ~ - ~ ' ~ � 9

36 \ 15 ~

- [ Z~ 5-6 - Clutch hrood 55 / r~ 4 - Clutch brood

- / �9 3 - Clutch brood / 0 2 - Clutch brood

L �9 1 - Clutch brood

I I I l I I

I 2 3 4 5 6

Rank order in which clutch was laid

Figure 4. Mean percentage hatching success of clutches of different rank order of spawning in broods comprising various numbers of clutches. Data indicate the average success of females that chose to spawn at least partly based on whether or not a male was tending embryos and, if so, had spawned only once or had already acquired many clutches. Sample sizes are numbers of female clutches.

extent, males have already mated (Fig. 3, Table IV). Surely this assumption underestimates the variance in female reproductive success. Hence the actual differences between male and female vari- ances and intensity of selection should be less than

estimated, given the greater likelihood that females choose mates partly on the basis of the number of clutches that they have already acquired (Fig. 4). Sexual differences in the expected lifetime repro- ductive success of individuals would be further

1154 Animal Behaviour, 35, 4

dampened by the younger average age at first reproduction and the generally higher adult sur- vivorship of females (DeMartini & Anderson 1980; Howard 1983).

D I S C U S S I O N

Benefit of Paternal Care

Paternal care of benthic, adhesive embryos is relatively common among teleosts compared to higher vertebrates (e.g. see Blumer 1979). The nature of care giving in teleosts ranges from indirect defence of embryos fertilized within the male's territory (Kodric-Brown 1983; Loiselle 1983) to passive or active defence of young (this study), to a complex repertoire of defence plus ventilatory and other sanitary activities (van den Assem 1967, and references therein). Fanning and related activities have not evolved in O. pictus probably because its small clusters of relatively small eggs are laid on exposed reef surfaces in a turbulent environment.

Relatively few field studies have experimentally tested the assumed benefit of paternal tending (e.g. Downhower & Yost 1977; Dominey 1981, cited in Bain & Helfrich 1983; Blumer 1985). The few existing data suggest that, as Emlen (1973), Wil- liams (1975), and others have theorized, defence by one parent may suffice for demersal eggs and non- motile fry (Perrone 1978; Blumer 1985; this study). Both parents may be necessary to protect and herd motile fry in some natural populations of cichlids (Barlow 1974; Perrone 1978) and, perhaps, other fishes (Perrone & Zaret 1979).

My presence may have attracted predators of embryos near control males in the orphaning experiment, and inflated losses. Even so, survivor- ship of embryos was nil when male parents were removed (Table II). Clearly, male care of offspring is necessary in this species.

Male Foraging Restriction

During tending, males were restricted to about one-fourth the area of reef that they frequented when not tending embryos. The average level of somatic decline was less severe for males that infrequently tended embryos than for those that tended embryos more often. Adult males also consumed less other prey than did females during

the breeding season (ANOVA: F = 4.0, df= 1,232, P < 0.05; Table III). Because females from outlying reef areas visit males for spawning (DeMartini 1985), females generally traverse greater areas of reef. The reduced opportunity to forage while tending embryos represents a definite cost for males and the threat of predation on untended embryos strongly influences males to restrict their move- ments (Table II).

Staying near the centre of the territory may also partly benefit the tending male who can remain ready to display to incoming females (DeMartini 1985). Probably, however, a more peripheral posi- tion in such small territories (mean radius approxi- mately five body lengths, DeMartini 1985) would not significantly reduce a male's ability to detect and court females.

Costs of paternal care in O. pictus might also include increased predation risk to the attendant male, but I have too few data on the survival of tagged males to evaluate this. Energy expended in embryo defence seems relatively minor, since active defence is infrequent (approximately 0"3 attacks/h; Table I).

Rohwer (1978) summarized some significant early evidence for the costs of male tending beha- viour. More recently, male mottled sculpins, Cottus bairdi, have been noted to decline greatly in body weight while tending embryos (Pedersen 1979, cited by Dominey & Blumer 1984). Townsend et al. (1984) and Sargent & Gross (1985) also evaluate the energy costs of paternal tending.

Filial Cannibalism Versus Heterocannibalism

The relatively infrequent, low incidence of canni- balism of embryos of early developmental stages by female O. pictus is consistent with heterocanniba- listic raiding (Rohwer 1978) of other females' embryos encountered on territories of males. If females attempt to cannibalize their own eggs (e.g. following disturbance, when eggs are eaten because they are likely to be lost to other predators of embryos, Bronstein 1982), they are usually unsuc- cessful at doing so. The relatively high average level of cannibalism of embryos by males must only partly reflect the heightened levels of raiding that are facilitated by dense packing into centralized spawning areas (Kynard 1978). More frequent cannibalism (of all embryo stages) by paternal males is ambiguous evidence for filial cannibalism. Since paternal males can both raid and cannibalize

DeMartini. Mating system of painted greenling 1155

their own young (but might only cannibalize their own young) and non-paternal males can only raid, either class of males might have a higher incidence of cannibalism.

The great overlap in similarity between tended and ingested embryos, coupled with the greater average incidence of pigmented-stage embryos in stomachs of parental-phase guardians, though, is strong evidence for frequent filial cannibalism. Site-restricted parental-phase males should have fewer opportunities to raid neighbours, and it is unlikely that they could successfully raid embryos more frequently from parental-phase than from mating-phase neighbours, particularly since raid- ing females do not. Males should guard late- development embryos more fiercely, since off- spring that are closer to hatching have higher reproductive value (Kynard 1978; Pressley 1981). It is also improbable that males would cannibalize their own unpigmented (rather than pigmented) embryos, because the energy content of the former is only minimally greater than that of the latter (Scrimshaw 1945). Then too, if tending males sometimes cannibalize eggs fertilized by neigh- bouring males on the tending male's territory (e.g. as in pupfish, Loiselle 1983), embryos should be eaten shortly after the stolen fertilization or at least before the development of pigmentation discour- ages prospective mates.

A male was usually present at or near its central site following the total loss of a single clutch, as it was three-fourths of the time throughout the breeding season ()~2=0.8, df= 1, P>0.15). Males that lost single clutches acquired an average of 2.2 clutches in their next breeding cycle. More frequent loss of single clutches than first clutches within multiple-clutch broods is neither the simple cause nor the result of desertion by males. More frequent total loss of single clutches thus suggests that paternal filial cannibalism also functions as a male courtship strategy. Consistent with this interpreta- tion, filial cannibalism of embryos has been noted in laboratory studies of sticklebacks (van den Assem 1967; Salfert & Moodie 1985), the nandid fish Badis badis (Barlow 1964), gouramis (Kramer 1973), paradise fish (DeNeff& Villars 1982), and in field populations of the bluegill sunfish (Dominey 1981, cited in Dominey & Blumer 1984), the damselfish Chromis notata (Ochi 1985), and the brook stickleback Culaea inconstans (Salfert & Moodie 1985).

Filial cannibalistic males, in essence, parasitize

the fecundity of females, whose lack of parental duties enables them to forage freely and maximize egg production (Emlen 1973; Williams 1975; Gross & Sargent 1985). Such paternal cropping can evolve (or not be overwhelmed by countervailing kin selection) if the benefit gained in subsequent broods outweighs the losses from the present brood (Rohwer 1978). I have shown that the mean hatching success of first-laid clutches increased from 19% (on average, 500 embryos) in broods of onc clutch to 79% (2000 embryos) in broods of three or more clutches. But the average 50 150 embryos found in the stomachs of tending males (Table III) are equivalent to less than 2-6% of an average clutch and perhaps one-half that much on a daily basis. Then, too, risk to filial cannibalism is spread among an average of three or four clutches within a brood, even if each clutch remains at risk for a number of days. Obviously, O. pictus is a species in which large numbers of eggs can be decremented by variable, small fractions of a clutch (DeMartini 1976; Rohwer 1978; Dominey & Blumer 1984),

Paternal cannibalism should be predisposed by polygyny, but the magnitude of cropping should be independent of mating success: a male of a given body size should cannibalize a given number of embryos regardless of the number of clutches acquired, since the energy cost of passive defence should be independent of brood size (Rohwer 1978; Perrone & Zaret 1979), and the duration of the parental phase is fixed by the embryo's develop- ment rate and temperature. Smaller males should crop fewer embryos per unit time spent tending; however, no data exist to test this. Larger male O. pictus defend spawning territories that are as small as (or smaller than) those of smaller males (DeM a r- tini 1976). Site restriction while tending thus might incur a greater energy cost for larger males. Larger- than-average males (greater than 177 ram: DeMar- tini 1985) in fact were in poorer somatic condition (somatic weight x 105/length-cubed) than smaller males (t = 2.90, N = 49, P < 0-001 ). The mean soma- tic condition of larger (greater than 191 mm) and smaller females did not differ (t=0.37, N=55, P>0.7).

I suggest that paternal filial cannibalism of embryos, in addition to heterocannibalistic raid- ing, typically serves to offset the restricted foraging opportunities imposed by site-dependent care. Raiding among neighbouring males is known to occur frequently in field populations of well-

1156 Animal Behaviour, 35, 4

studied species in which embryos are tended by males within aggregations (e.g. sticklebacks, Kynard 1978; sunfishes, Keenleyside 1972). Filial cannibalism may be no less common, only more difficult to document.

Mating Success, Reproductive Success and the Mating System

Downhower & Brown (1981) have shown that, in the mottled sculpin, the absolute hatching success of male-tended embryos increases with the number of embryos acquired. Male tending of more than one clutch confers the general advantage of reduc- ing the average predation loss for each clutch in the brood (Rohwer 1978; Dominey & Blumer 1984). Such a safety-in-numbers effect (McKaye 1981; Ridley & Rechten 1981) occurs if the average percentage of predation decreases with the number of clutches present in the brood, regardless of whether the major sources of embryo loss are conspecific females (Downhower et al. 1983) or neighbouring males and male filial cannibals (this study).

The painted greenling data on relative (per clutch) hatching success are the first to demonstrate an average advantage to polyandrous female fish that spawn with polygynous males (Fig. 3). The data of Downhower & Brown (1981, Fig. 5-5) indicate that female mottled sculpin generally benefit from spawning with tending males; this is a synchronous breeder whose females produce only one clutch of eggs per year (Downhower & Brown 1981).

Downhower & Brown's (1981, Table 5-3) data further suggest an effect of clutch sequence on the probability of hatching that is superficially similar to my data for painted greenling (Fig. 4). Down- hower & Brown (1981) attribute the decline in hatching success of late-laid clutches of the mottled sculpin to an increase in the proportion of terminal spawnings later in the season; in mottled sculpin, the sequence of clutch deposition is important, but the period within the spawning season is not (Downhower & Brown 1981; Downhower et al. 1983).

Brood size and sequence of clutch deposition also overwhelms subseasonal effects on hatching success in painted greenling (Fig. 4, Table V). However, unlike the mottled sculpin, painted greenling of varying sizes (ages) produce more than one clutch during protracted breeding seasons

(DeMartini & Anderson 1980). Mixed-sized fish of both sexes are simultaneously reproductive, and females (and, as a result, males) are highly asynch- ronous. At a particular reef, there is a relatively broad (several-months) period during which equi- valent probabilities exist for successfully producing planktonic larvae from tended embryos. Female O. pietus are undoubtedly asynchronous as a result of age (size) effects on the timing of spawning, because populations comprise numerous age classes (DeMartini & Anderson 1980).

Asynchrony promotes polygyny in male-tending fishes (Downhower & Brown 1981) and many other organisms (Thornhill & Alcock 1983). Protracted spawning in O. pietus, and the resulting heightened asynchrony among males and females, have further reinforced selection for polygamy. The lengthy site- restricted tenure of tending males, necessitated by predation threat to the embryos, incurs an energy cost that can, in part, be overcome by filial cannibalism. Moreover, the benefit of polygyny to individuals of both sexes, integrated over the protracted spawning season, can more than com- pensate for additional, relatively small losses of embryos from paternal cropping. Single-clutched, more synchronous and briefer-spawning species of male tenders like the mottled sculpin cannot subsi- dize the energy cost of male-tending in this manner (Downhower et al. 1983). Populations of synchro- nized breeders in food-rich environments also do not have filial cannibalistic males, even though asynchronously spawning populations of the same species in food-poor environments may have filial cannibalistic males (Whoriskey & FitzGerald 1985).

Determinants of Male Breeding Cycles

A female-receptive (mating or sexual) phase followed by a non-receptive (parental) phase are normal components of male breeding cycles in many groups of teleost fishes that have paternal care (e.g. centrarchids, Gross & Nowell 1980; darters, Grant & Colgan 1984; damselfishes, Ochi 1985; wrasses, Potts 1974; gobies, Cole 1982; sticklebacks, Kynard 1978; but also see Mertz & Barlow 1966). Cyclical receptivity is due to males refusing more eggs (females) than they can tend, whether because of restricted amounts of spawning substrate or temporal constraints on physiological ability to tend embryos (Williams 1975; Loiselle & Barlow 1978; Blumer 1979).

DeMartini: Mating system o f painted greenling l 157

In O. pictus, the average ha tching success of clutches increased monotonica l ly with the numbers of clutches acquired, up to b rood sizes of f iv~s ix clutches (Fig. 1). An apparen t asymptote in mean percentage h a t c h i n g success existed at greater numbers of clutches; a decline in ha tching success in the largest broods is equivocal (Fig. 1). The data nonetheless suggest tha t male O. pictus rarely acquire more than a threshold n u m b e r of clutches per breeding cycle because they canno t physiologi- cally remain to guard addi t ional clutches. In addit ion, females avoid highly polygynous males tha t are mos t likely to cannibal ize the clutches of la te-spawning females. Substrate l imitat ion seems unlikely because mult iple-clutch b roods occupy a max imum of less than 5% of the reef area within the male 's territory.

A C K N O W L E D G M E N T S

I gratefully acknowledge the advice and encourage- men t of R. Paine, D. Paulson, G. Orians and especially S. Rohwer, and thank them for their critiques of various drafts. I also t hank L. Blumer, J. Dixon, J. Downhower , M. Gross, A. Harpe r and several anonymous reviewers for construct ive criti- cisms of later drafts; J. Lehnen and J. Joseph for typing drafts; and K. Fisher for prepar ing the final manuscript . This study was initially funded by a 1970 1973 predoctoral fellowship from the Nat io- nal Science F o u n d a t i o n and represents par t of a dissertat ion in zoology at the Universi ty of Wash- ington.

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(Received 3 April 1986; revised 7 July 1986; MS. number: a4647)