Latitudinal Effects on Juvenile Size and Fecundity in <I>Petaloconchus
Total Page：16
File Type：pdf, Size：1020Kb
BULLETIN OF MARINE SCIENCE, 45(2): 369-376, 1989 LATITUDINAL EFFECTS ON JUVENILE SIZE AND FECUNDITY IN PETALOCONCHUS (GASTROPODA) Michael G. Hadfield ABSTRACT Adult tube diameters, embryonic capsule dimensions, and hatching juvenile shell lengths are about 25% larger in the more northerly of two populations (Washington and California) of the sessile vermetid gastropod Peta/oconchus montereyensis. The proximate cause of the size differences between the two populations is apparently the lower annual temperature in Washington waters which results in larger adult females. Their larger capsule glands produce larger capsules containing more eggs, but egg diameters are the same as in the southern population. Thus the number of eggs per capsule is significantly greater in the northern population and, since capsules typically produce a single juvenile snail with all but one egg serving as nurse yolk, this explains the greater size of San Juan Island juvenile snails. The num ber of capsules brooded at one time is similar in the two populations. Thus, while northern females do produce more eggs, as expected for larger animals, they sacrifice increased fecundity for significantly increased juvenile size. Plausible explanations include a wide range of tol- erable variance around an optimized settling size in the species, a range in the size of selection agents paralleling the latitudinal cline of differences, and selection for increased hatching size to stabilize developmental time between hatching and sexual maturity. The proximate chain of relationships delineated here leads to very different results than are usually predicted by life-history theory: fecundity does not increase with body size; egg size does not predict developmental mode or hatching size; body size seems to have little to do with developmental mode. Clearly, different mechanisms for supplying developmental nutrition can lead to very different suites of life-history traits, and a priori assumptions of trade-offs can lead to false predictions for many species. A life-history characteristic often assumed to be among the optimization effects of natural selection in benthic marine invertebrate animals is the size of the juvenile as it first assumes the mode oflife of the adult (Christiansen and Fenchel, 1979). This is the "settling size" or "size at metamorphosis" for species with pelagic, larval development and "hatching size" for species with benthic, direct development. Obviously, in the absence ofa planktotrophic growth phase, settling size is the same as hatching size. Variation in hatching size occurs in many species, especially marine prosobranch gastropods, often as a consequence of nurse-egg consumption by embryos during intracapsular development (Thorson, 1946; Spight, 1976). Either competition for nurse eggs is unequal within a capsule or the ratio of nurse eggs per embryo varies between capsules, broods, or even populations (Spight, 1976; Rivest, 1983). Because of nurse-egg utilization, many species do not meet expectations based on typical life-history character interac- tions like egg size and developmental mode. Typically, small eggs are associated with pelagic, planktotrophic, larviparous development and large eggs with the opposite character set; however, when some eggs are eaten by capsule mates, the result can be benthic development in combination with small ova. In fact, when nurse eggs are present, they eliminate the potential for prediction of hatching size, developmental mode, and fecundity which are often made on the basis of tax- onomy, egg size or adult size. Within populations of the western North American vermetid gastropod Petal- oconchus montereyensis some variation in hatching size occurs as a result of varying nurse-egg to embryo ratios among capsules (Hadfield, 1966), but a greater 369 370 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989 and more interesting difference occurs in the sizes of hatching juveniles from different geographical regions. The initial observation was that newly released juveniles of P. montereyensis from San Juan Island, Washington were distinctly larger than those from Monterey Bay, California. The work described here began in an effort to quantify this size difference and to ascertain its immediately un- derlying causes. The questions addressed were: (1) how different are the sizes of hatching juveniles in the two locations; (2) does the difference in juvenile size arise from variation in egg size or allotment of nurse eggs; and (3) are there concurrent differences in adult sizes? Analyses revealed an unexpectedly tight coupling between a usually unrelated pair of life-history traits, adult size and hatching size. This coupling arises through the mechanism of apportioning nurse eggs, which is to some degree further clarified. Finally, these results led to an analysis offecundity, specifically to a comparison of brood sizes in the California and Washington populations of P. montereyensis. These data test hypotheses of life-history evolution concerned with the effect of body size on fecundity, a re- lationship usually found to be positive (Thompson, 1979; Hughes and Roberts, 1980; Hines, 1982; Perron, 1983; 1986). MATERIALS AND METHODS Specimens of Petaloconchus montereyensis were collected from the intertidal zone at the Hopkins Marine Station, Pacific Grove, Monterey Bay, California (36°37.5'N; 121°55'W) and from the west coast of San Juan Island, Washington near Limekiln Lighthouse (48°31 'N; 123°IO'W). These two locations lie very near the souIhern and northern limits of the distribution of this species (based on personal observations). All specimens used in the study were collected from rocky intertidal habitats near or slightly below the zero tidal level. Specimens collected by SCUBA from depths of about 10 m at Pacific Grove did not differ significantly from the intertidal ones. Searches of subtidal areas at San Juan Island have not revealed specimens of P. montereyensis. Reproductively active specimens have been collected in all seasons of the year at both locations. Specimens were compared to further understand the differences between hatching sizes of juveniles from the two locations. Adult comparisons included color and morphology, but were mainly devoted to measurements of shell apertures of larger animals (referred to as tube diameter because vermetid shells, uncoiled and cemented to the substratum, take the form of elongate, vermiform tubes with circular apertures). Measurements were made to 0.0 I mm with the aid of an ocular micrometer in a binocular dissecting microscope. After measurement, shells of adult P. montereyensis were carefully cracked along their entire lengths with long-nose pliers and the shell fragments were removed with fine-tipped forceps. Females were easily distinguished by the long row of brooded, ovoid embryonic capsules that could be observed through the pallial wall. The mantle was opened lengthwise and the capsules removed. The transparent capsule membranes allowed ready observation of the capsule contents. Most females brooded a variety of developmental stages, ranging from uncleaved ova to ready-to-hatch juveniles. The number of capsules brooded was recorded along with the shortest and longest diameters of all of the capsules brooded by each female. Capsules, ova and embryos were measured to the nearest 0.01 mm with an ocular micrometer in a binocular dissecting microscope. After measurement, capsules containing undivided ova were carefully opened by tearing them with fine-tipped forceps, and the eggs were removed and counted. Several ova from each capsule were measured to determine mean diameter. Shell lengths of ready-to-hatch juveniles (determined by the absence of the velum and internal yolk and the presence of well developed coloration) were measured and their size-frequency distribution plotted. Data on egg diameter, juvenile-shell length, capsule volume (calculated as the volume of an ovate spheroid) and adult aperture diameter were reduced to simple means and standard deviations, and measurements from the two populations were compared by {-tests. The relationship between capsule size and female size was analyzed using the modal capsule volume of each brood because within-female variance in capsule volume was great; modal volume did not differ greatly from mean volume in most cases. RESULTS Newly hatched juvenile snails from San Juan Island, Washington ranged in length from 1.30 to 1.61 mm with an average of 1.45 mm; those from Monterey, HADFIELD: LATITUDINAL SIZE DIFFERENCE IN JUVENILE SNAILS 371 Tab[e I. Comparison of adult and developmental characters of Petaloconchus rnontereyensis from San Juan Is[and, Washington (SJI) and Monterey Bay, California (Mont.). (x, mean; SD, standard deviation; N, number measured or counted; R, range of measurements) Character SJI Mont. Prob,· Adult tube diameter x 2.03 mm 1.62mm *** SD 0.12 0.10 N 16 2[ R 1.63-2.17 1.36-1.75 Capsule volume x 0.34 mm3 0.18 mm3 *** SD 0.07 0.03 N 142 185 R 0.20--0.50 0.1 [-0.25 Eggs per capsule x 372 233 *** SD 71 44 N ]6 ]4 R 258-499 164-307 Hatching shell length x 1.45 mm 1.18 mm *** SD 0.08 0.06 N 74 46 R 1.30-1.61 1.05-1.30 Egg diameter x ] ]2/Lm 11O/Lm n.s. SD 7.47 5.75 N 16 33 R 101-]25 ]04-]20 Capsules per brood x ]4.88 [7.05 n.s. SD 5.24 8.84 N 17 2] R 8-23 3-33 • Probability: ••• < < <0.001; n.s. >0.1. California ranged from 1.05 to 1.30 mm and averaged l.l8 mm (Fig. 1). These differences were statistically significant (Table I). The larger juveniles from the Washington population arose, as expected, from larger capsules (Table 1). More than 90% of embryonic capsules observed from both populations of Petaloconchus montereyensis held only a single embryo, and the question thus became: is the larger juvenile size at San Juan Island a result oflarger eggs or a greater investment of nurse eggs per capsule? A comparison of egg diameters in the two populations showed them to be about 110-112 /-Lm in both while numbers of eggs per capsule were significantly different (Table 1).