Invertebrate Reproduction and Development, 22:1-3 (1992) 193-202 193 Balaban, Philadelphia/Rehovot 0168-8170/92/$05.00 © 1992 Balaban
Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species
RAYMOND T. BAUER Center for Crustacean Research, Department of Biology, University of Southwestern Louisiana, Lafayette, Louisiana 70504-2451, USA
Summary
Study of latitudinal variation in seasonality of reproduction and recruitment of benthic marine invertebrates is useful in generating and testing hypotheses about causal factors acting on reproduction such as temperature and larval food supply that might be altered by changes in world climate. Analysis of latitudinal variation in reproductive patterns might be made with comparisons (a) among species with a common phylogenetic history from different latitudes and habitats and (b) among phylogenetically different taxa from the same location. Hypotheses on variation of reproductive seasonality with latitude are tested here with results of a study on nine species of caridean and two species of sicyoniid shrimp sampled from a tropical seagrass meadow in Puerto Rico. Breeding condition was determined by the presence or absence of incubated embryos (carideans) and the state of ovarian development in both carideans and sicyoniids. Recruitment was estimated from the percentage of individuals of monthly population samples in the juvenile size classes. Comparison of reproductive patterns among tropical, subtropical, and cool temperate Sicyonia spp. supports the paradigm of continuous reproduction in the tropics with increased restriction of breeding season with an increase in latitude. A greater intensity of breeding effort appears to accompany the shorter breeding period associated with an increase in latitude. At the tropical site most females of all caridean species carried embryos during all months of the year. With the onset of sexual maturity, caridean females produced consecutive broods for the rest of their relatively short (< 6 month) life span. In both sicyoniid and caridean species, recruitment occurred throughout the year but was highly variable, i.e., episodic rather than truly continuous or seasonal. Patterns of recruitment were highly concordant among but not between sicyoniid and caridean species, indicating that different sets of environmental factors controlled recruitment in the two groups. It is suggested that simultaneous study of adult reproduction and larval ecology is necessary to understand patterns of reproduction and recruitment. Coordinated effort on a global scale in studying latitudinal variation in reproduction and recruitment is suggested in order to predict the consequences of climate change on commercially and ecologically important marine invertebrate species.
Economic and Applied Aspects of Invertebrate Reproduction. Proceedings of the Sixth International Congress on Invertebrate Reproduction, Trinity College, Dublin, 28 June - 3 July 1992. 194
Introduction to temporal patterns of plankton productivity in which the duration of high productivity is negatively corre Making generalizations about biological phenome lated with latitude. Thus, reasoning from Thorson's na from empirical studies is a useful and necessary ideas, at low latitudes there is relatively little varia tool for summarizing information on those phenome tion in primary and secondary productivity (larval na. More importantly, such generalizations or general food supply) throughout the year in coastal areas, and principles serve a heuristic function by acting as a there is little selection for seasonality in reproductive model or paradigm for making and testing hypotheses cycles. At higher latitudes (temperate, boreal), breed on causal factors or selective pressures that may be ing seasons and peak larval output should roughly responsible for the patterns observed. Quite often coincide with the seasonal pulses of productivity. The generalizations are oversimplifications that do not situation is more complex in polar regions where hold up as more studies are conducted on the biologi temperature variation is again slight. Although prima cal phenomenon of interest and contradictory results ry and secondary productivity in the plankton is high are encountered. The paradigm is then either discard ly seasonal, restricted to intense bursts in the polar ed or modified, but in the process new, often impor summer, current information shows that reproduction tant information is discovered, and our understanding of invertebrates with planktotrophic larvae is not of the biological world increases. necessarily highly seasonal and correlated with the Generalizations about latitudinal variation in summer pulse of planktonic productivity (Pearse et annual patterns of reproduction in near-shore, benthic al., 1991; Thorson, 1950). marine invertebrates have been useful in suggesting Although reviews and summaries of the literature the underlying environmental factors that might ac on marine invertebrate reproduction certainly do count for the patterns observed. Orton (1920) hypoth seem to indicate a tendency for extended reproductive esized that relatively constant temperature conditions seasons at lower latitudes, with more restricted ones in tropical seas with high water temperatures year- at higher latitudes, there are certainly many excep round was the cause of continuous reproduction in tions reported [see reviews for invertebrates in gener populations of a variety of tropical marine inverte al in Giese and Pearse (1974); for crustaceans in Sas- brates. Seasonal variation in water temperature, the try (1983)]. Thus, there are tropical taxa in which pattern of which is strongly tied to latitude, has al different species may either have seasonal or continu ways been considered an important proximate factor ous breeding (Cameron, 1986; Hendler, 1979). Trop or environmental stimulus in triggering and maintain ical reef corals often have restricted breeding periods ing gametogenesis and thus defining the breeding (Harrison et al., 1984; Schlesinger and Loya, 1985). season of marine invertebrates as well as other marine Some tropical species have semiannual breeding and terrestrial animals. Thorson (1950) suggested that seasons in areas subject to major semi-annual envi the important selective pressure acting on timing of ronmental perturbations, i.e., monsoons (Giese and reproduction in marine invertebrates with planktotro- Pearse, 1974). phic larvae might be the temporal variation of larval Thus, general or simplistic models about the rela food supply, that is, the seasonal pattern of primary tionship between length of breeding pattern and lati and secondary productivity. Thus, the temporal avail tude may not be applicable to all or most near-shore ability of larval food supply was supposed to be the benthic invertebrates. There probably is no one gen "real" reason ("ultimate factor"; Baker, 1938) for the eralization about reproduction or recruitment that can observed seasonality (or lack thereof) in reproduction be made about all or most taxa. The term "near-shore and larval output in benthic invertebrates. Tempera benthic invertebrate" refers to a variety of taxonomic ture (and/or other environmental variables) act as groups with very different phylogenetic histories, environmental cues ("proximate factors") on the each taxa with its own reproductive capabilities and physiological systems of these benthic invertebrates. constraints imposed by its particular body plan, physi By means of these cues, spawning of eggs or release ology, and ecology. At similar latitudes there may be of planktotrophic larvae is timed to coincide with much variation from one benthic habitat to another in periods of favorable food supplies in the plankton. a variety of abiotic and biotic factors that influence Thorson's (1950) classic paper presented evidence reproductive patterns. for several invertebrate groups that the breeding A corollary to the hypothesis of a latitudinal gradi season became more restricted or seasonal with an ent in breeding and larval production of near-shore increase in latitude. As noted above, he attributed this invertebrates is that recruitment patterns should mir- 195 ror (with a suitable lag period) reproductive patterns, (seagrass meadows) in a tropical locale, Puerto Rico, i.e., continuous recruitment in tropical latitudes with West Indies, based on data reported in Bauer (1989) increasing seasonality of recruitment with an increase and Bauer and Rivera Vega (1992). In addition, com in latitude in temperate and boreal latitudes (Bauer, parisons will be made among Sicyonia species from 1989), The caveat expressed above about compari this tropical locale (Bauer and Rivera Vega, 1992) sons of reproductive patterns among different taxa and Sicyonia spp. from other latitudes using data also applies to recruitment. Different taxa may have taken from other studies (Anderson et al., 1985; planktotrophic larvae that are affected by very differ Kennedy et al., 1977). These comparisons are made ent pressures in the plankton (e.g., disparate food possible because the intensity of sampling and the supplies, predators) that may influence larval success methods of estimating reproductive activity were and recruitment in a variety of ways. As larvae arrive similar among the three studies cited. at the juvenile and adult habitat, benthic predators may be acting differentially on the larvae and post- larvae as they settle and metamorphose during re Data Base cruitment into the benthic population of the species. Populations of shrimps were sampled monthly for Perhaps the most constructive approach to an analy sis of the relationship between seasonality in repro one year in seagrass meadows, composed of turtle duction and recruitment with change in latitude would grass (Thalassia testudinum) and manatee grass be to make comparisons that factor out, as much as (Syringodium filiforme), located at Dorado (18°N, possible, variation due to differences in (a) phylo- 66°W), on the north coast of Puerto Rico, West genetic history and (b) habitat. Thus, one might study Indies. Samples were taken with pushnets both during and compare temporal patterns in reproduction and the day and night, but the vast of majority of individu recruitment (1) among (relatively) unrelated taxa als for all species were captured at night when the from similar latitudes and habitats, i.e., species that shrimps and other macroinvertebrates are most active. experience similar environmental pressures but which Nearly 75,000 caridean shrimps were collected be have separate phylogenetic histories and/or (2) among longing to 18 species (Bauer, 1985a). Nine species (relatively) closely related taxa from different lati accounted for 99.9% of this abundance (Table 1), and tudes and/or habitats, i.e., species with a common the reproductive and recruitment patterns of these phylogenetic history exposed to dissimilar environ species were analyzed (Bauer, 1989). Approximately mental pressures. Thus, differences in breeding and 7,500 penaeoid shrimps were collected, and 85.9% of recruitment patterns among unrelated taxa from the these individuals belonged to two species, Sicyonia same sampling site might be attributable to taxon- parri and 5. laevigata (Bauer, 1985b) whose breeding specific reproductive and recruitment capabilities and and recruitment patterns were reported in Bauer and constraints. Among closely related species from Rivera Vega (1992). different latitudes or habitats, variations in reproduc For the carideans the index of breeding activity tion and recruitment might be ascribed to major envi used was the percentage of adult females that were ronmental factors that vary among sampling sites. ovigerous, i.e., incubating fertilized embryos. Stage In this report I use the approach outlined above to of ovarian maturity on a scale of 1 (no development) compare and contrast reproduction and recruitment to 4 (ovary full of large vitellogenic eggs, female near between two relatively unrelated groups of decapod spawning) was also observed and recorded for fe crustacean shrimps, sampled at the same location, males (Bauer, 1989). In the sicyoniid (penaeoid) with distinct modes of reproduction. Caridean shrimps in which females do not incubate embryos, shrimps, like all pleoeyemate decapods (crayfish, the ovarian maturity (immature versus mature, based lobsters, crabs), incubate their embryos to advanced on visual estimates of relative frequency of postvitel- zoeal larvae. In contrast, penaeoid shrimps (Deea- logenic eggs) was recorded for all females examined poda, Dendrobranchiata) spawn eggs that are immedi (Bauer and Rivera Vega, 1992). ately fertilized and released into the plankton where In each caridean species females were defined as embryonic development takes place, after which they "adult" (potentially capable of reproducing) if they hatch as relatively undeveloped nauplius larvae. I will were as large or larger than the smallest female ob make comparisons of reproductive and recruitment served carrying embryos. In Sicyonia spp. adult patterns among and between nine species of carideans females were those as large or larger than the smallest and two penaeoids (Sicyonia) from the same habitat female observed with a mature ovary. 196
Table 1. Comparison in caridean and Sicyonia (Penaeoidea) out a recognizable seasonal component. Furthermore, shrimp species in monthly values for percentage of adult it was possible to determine if females carrying em females with mature ovaries bryos were developing another batch for spawning after the current brood of incubated embryos hatched. Perc sntage of adult females This was done by recording the stage of ovarian with mature ovaries development and stage of embryonic development in females from samples and observing the pattern of Species Med ian Min Max N hatching and spawning in captive females. In all Caridea: species observed the sequence of events in live ovig Alpheus normanni 16 0 35 588 erous females was hatching of embryos, a molt within Latreuies fucorum 24 15 56 1147 a day or two of hatching, and subsequent spawning of Leander lenuicornis 24 0 56 184 the eggs in the mature ovary within a day or two of Processa bermudensis 28 13 55 468 the post-hatching molt. In preserved material there Hippolyte curacaoensis 28 9 46 601 was a statistically significant correlation between Processa riveroi 30 29 70 198 stage of ovarian maturity and stage of embryonic Latreutes parvulus 38 12 80 502 development in all species. Thus, as a brood of previ Periclimenes 40 23 60 486 ously spawned embryos was being incubated, the americanus ovary of most females matured so that a new spawn Thor manningi 43 32 84 466 took place soon after hatching of the embryos, female molting, and mating (there is no sperm storage in Penaeoidea: these carideans). Periods between spawns varied from Sicyonia parri 13 0 26 848 1-2 weeks in these species. Reproduction in these Sicyonia laevigata 26 0 42 456 small seagrass carideans can be characterized as both continuous and intense, both at the level of the popu min, minimum; max, maximum; N, total number of adult lation and the individual. Cohort analysis of some of females examined. the species indicated that female life span on the seagrass meadows is a matter of months, certainly Recruitment was defined as the entry of individu much less than a year (Bauer, 1986; Rivera Vega, als from the plankton into the juvenile and adult 1985; Salva, 1984), probably due to the intense fish shrimp populations in the seagrass beds. Monthly predation that occurs on small macroinvertebrates in seagrass meadows (Heck and Orth, 1980; Randall, recruitment was estimated by calculating from 1967). monthly size frequency distributions the proportion of the population in the "juvenile" size classes, which were defined as the lower 25% of all possible size The index of breeding intensity or activity differed for the carideans (percent adult females incubating classes observed in that species. The upper size limit embryos) (Bauer, 1989) from that used for the sicyo defined in this way for "juveniles" approximately niids (percent adult females with mature ovaries), as coincided with the size of male and female sexual the latter do not incubate embryos (Bauer and Rivera maturity in both the caridean and sicyoniid species Vega, 1992). I have calculated values for percentage (Bauer. 1989; Bauer and Rivera Vega, 1992). of adult females with mature ovaries (stages 3 and 4) for the caridean species for comparison with sicyoniid species in which "mature" (dominated by large post- Comparisons among Caridean and Sicyoniid vitellogenic eggs) ovaries were used as the indicator Species at the Same Tropical Location of reproductive activity (Table 1). The median, mini mum, and maximum values for the caridean species Bauer (1989) analyzed reproductive patterns of the are generally higher than those of the two sicyoniid nine caridean species listed in Table 1 based on the species (Table 1). percentage of adult females incubating embryos. A relatively high percentage of adult females in all What might account for the apparently higher level species were ovigerous throughout the year. Statisti of reproductive intensity in terms of ovarian develop cal tests for possible concordance among species in ment of the carideans relative to the sicyoniids? One highs and lows of this estimate of breeding showed no might first ask if the values are comparable. Is the common pattern. Thus, on the population level re period for ovarian development, i.e., period between production was continuous throughout the year with spawns, shorter in carideans? The time interval be- 197
tween spawns varied from 1-2 weeks in females of same habitat, with the duration of periods between the nine caridean species. Although the period of an spawns similar or perhaps somewhat longer than that ovarian cycle in the tropical Sicyonia species is un for the carideans. However, the survivorship of an known, it is doubtful that it could be shorter than that individual fertilized egg put immediately into the determined for the carideans. Anderson etal. (1985), plankton by a Sicyonia female is probably less than for instance, reported a mean period of 19 days be that for any individual caridean embryo. The sicyo tween spawns in Sicyonia ingentis. If the duration of niid embryo, starting out at the zygote stage, must ovarian development is longer in the sicyoniids than develop completely in the plankton to hatching as a that given for the carideans, or if ovarian cycles are nauplius larva, which then must develop through all not continuous as in the caridean species, then the the larval stages to the postlarva which will settle out intensity of reproductive effort, as estimated in of the plankton as a recruit into the benthic population Table 1, would appear lower than that of the cari of the seagrass meadows. The caridean embryo, on deans. the other hand, is cared for by the female throughout However, reproductive effort per spawn in terms of its embryonic development and hatches as an numbers of fertilized eggs produced is probably advanced zoeal larva that will spend much less time greater in the sicyoniids than in the carideans. The subject to the vagaries and dangers of the planktonic incubatory caridean females produce larger eggs and environment before settlement into the seagrass mead fewer embryos than do the free-spawning sicyoniids. ows. Thus, given the trade-offs among number of Egg size at spawning was 240-440/t in the nine cari embryos produced per spawn, number of spawns per dean species (Bauer, 1991) compared with approxi reproductive lifetime, presence or absence of parental mately 200ft in the two Sicyonia spp. The median care, and duration of time spent by larvae in the number of embryos per brood (spawn) in the nine plankton, it is probable that the sicyoniids and cari caridean species varied from 56-600 and was less deans from the tropical seagrass habitat have similar than 100 in five species (Bauer, 1991). The number of reproductive effort. eggs spawned by the Sicyonia spp. has not been mea The evidence thus indicates that, once sexual sured, but in the much larger S. ingentis the mean maturity is reached, females of both groups go number of eggs per spawn was 86,000 (Anderson et through continuous cycles of ovarian maturity and al., 1985). Even scaled down for the differences in spawning until they die, probably through predation, size of adult sicyoniid females (Table 2), it is likely after a life span of a few to several months (less than that the number of eggs spawned in the tropical Sic one year) after arriving at the seagrass meadows. yonia is at least an order of magnitude larger than that Settlement can occur during anytime of the year (see for the comparably sized carideans. "Recruitment Patterns..." below). Thus, an individu al female cannot "track" any particular season that might be more favorable to breeding, and there can be Table 2. Relationship between size (carapace length) and no selection for seasonality in breeding patterns. longevity of females in Sicyonia species from three different latitudes (biogeographical areas)' Additionally, it may be that there is little or no pre dictable variation in mortality in the larval (plankton ic) environment so that there would be no selection Species Size range of Longevity adult female (months) for breeding during any particular time of the year. (mm CL) Although the caridean and sicyoniid shrimps have very different phylogenetic histories and reproductive S. parri 3-9 6-8 physiologies, the common selective pressures of the S. laevigata tropical environment in which they co-occur, perhaps (tropical) together with their short life spans, appear to have S. brevirostris 17-35 20-22 produced a similar pattern of continuous, non-season (subtropical) S. ingentis 24-45 >22? al reproduction. (cool temperature) Latitudinal Comparisons in Reproductive Patterns of Sicyoniid Shrimps
Sicyonia spp. may thus be putting out many more In this section I compare temporal patterns in fertilized eggs per spawn than carideans from the reproduction among Sicyonia spp. from different 198 latitudes. The intensity of sampling and methods for A S. ingentis (cool temperate) estimating breeding activity (percentage of females with mature ovaries) are comparable among the tropi • S. brcviroslris (subtropical) cal species Sicyonia parri and S. laevigata from sea- Y S. parri (tropical) grass meadows in Puerto Rico (18°N; Bauer and
international agencies will be important in order to Bauer, R.T., Analysis of embryo production in a caridean supply the personnel, funding, and material support shrimp guild inhabiting tropical seagrass meadows. In; needed for such a major but essential undertaking. Crustacean Egg Production, A. Wennerand A. Kuris, eds.,BalkemaPress, Rotterdam, 1991, pp. 181-192. Bauer, R.T. and Rivera Vega, L., Pattern of reproduction and recruitment in two sicyoniid shrimp species Acknowledgements (Decapoda: Penaeoidea) from a tropical seagrass habi Numerous students in the Department of Biology, tat, J. Exp. Mar. Biol. Ecol., in press. University of Puerto Rico, Rio Piedras, provided Burkenroad,M.D.. The evolution of the Eucarida (Crusta invaluable assistance in the field and in the laboratory cea, Eumalacostraca) in relation to the fossil record, Tulane Stud. Geology, 2 (1963) 3-16. during the work on tropical seagrass shrimps. 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