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Oer 9 Springer-Verlag 1982 Oecologia (Berl) (1982) 54:348-352 Recruitment of Marine Invertebrates: the Role of Active Larval Choices and Early Mortality Michael J. Keough and Barbara J. Downes Department of Biological Sciences, University of California, Santa Barbara, Ca 93106, USA Summary. Spatial variation in the recruitment of sessile marine invertebrates with planktonic larvae may be derived from a number of sources: events within the plankton, choices made by larvae at the time of settlement, and mortality of juvenile organisms after settlement, but before a census by an observer. These sources usually are not distinguished. A study of the recruitment of four species of sessile invertebrates living on rock walls beneath a kelp canopy showed that both selection of microhabitats by settling larvae and predation by fish may be important. Two microhabitats were of interest; open, flat rock surfaces, and small pits and crevices that act as refuges from fish predators. The polychaete Spirorbis eximus and the cyclostome bryozoan Tubulipora spp. showed no preference for refuges , but settled apparently at random on the available substrata. Tubulipora was preyed upon heavily by fish, while Spiro~rbis was relatively unaffected. The bryozoans Celleporaria brunnea and Scrupocellaria bertholetti both recruited preferentially into refuges. Scrupocellaria were preyed upon, while Celleporaria juveniles seemed unaffected. Predation by fish modified the spatial distribution (Tubulipora), abundance (Tubulipora), or size distribution (Scrupocellaria) of the juvenile population, or had relatively little effect (Cellepor- aria, Spirorbis). All of the above events occur within three weeks of settlement. Since inferences about the effect of larval events on the population dynamics of adult organisms are often based on observations of the patterns of recruitment after one or two months, they are therefore likely to be misleading. Introduction. The colonisation of habitats by marine organisms with planktonic larvae involves three phases: development (including dispersal as a planktonic form), testing of a habitat for suitability, and settlement (summarised by Underwood 1979). For sessile invertebrates, the latter phase also includes attachment to the substratum and metamorphosis. The organism is unlikely to be detected immediately, because of small size, cryptic habitat, etc., and there is a fourth "phase", survival until the organisms is counted by an observer. This phase may last from hours to months (Scheltema 1974), but it is not a true life-history stage, merely Offprint requests to." M.J. Keough 0029-8549/82/0054/0348/$01.00 a reflection of the limitations of the observer. The number of organisms passing through the fourth phase is termed recruitment, while the number passing to the third phase is termed settlement. Recruitment is a composite of larval and juvenile stages, while settlement involves only larval stages. It is important to distinguish between settlement and recruitment. Non-random patterns of recruitment, such as differences in the density of recruitment with height on the shore (Underwood 1979) or differences in the density of recruitment with patch size (Jackson 1977; Keough 1982a), or with microhabitat, may have two causes: (1) differential settlement, and (2), different probabilities of early mortality in different parts of an organism's habitat. The first may involve an active response by larvae at the time of settlement that may be an evolved response to patterns of mortality, while the second involves no active choice by larvae. Failure to distinguish between these two phenomena may lead to misleading inferences in a number of areas. First, explanations for the spatial distributions of adult organisms have frequently neglected the importance of recruitment (Underwood and Denley 1982), and second, many of the studies that have included recruitment in the interdidal zone of rocky shores, have not distinguished between recruitment and settlement. This may have led to an overestimation of the importance of interactions between adult organisms and physical factors in limiting these distributions. The same is true of work on subtidal hard substrata; the terms recruitment and settlement are used interchangeably, when recruitment is actually measured. Patterns of recruitment have then been used to make inferences about larval settling behaviour (e.g. Day and Osman 1982; Dean and Hurd 1980; Jackson 1977; Osman 1977; Schoener and Schoener 1981). At the community level, it has been suggested for some subtidal systems, species arriving first may be able to resist further invasion by other species, so that the abundance of sessile species in such communities can be explained by measuring the colonising ability of component species (e.g. Dean and Hurd 1980; Sutherland and Karlson 1977). It is often considered that the ability of a species to colonise a habitat can be measured accurately by its recruitment rate (usually over a time period of 1-2 mo.). In a similar way, many other studies have considered the effect of predation in natural communities (e.g. Day 1977; Day and Osman 1982; Keough and Butler 1979; Osman 1977; Paine 1966; Russ 1980; Sammarco 1980). 349 Most have used exclusions (cages, fences, etc.) that modify the physical environment, such as light, water flow, sedimentation, in some way. Differences in the abundance of taxa between controls and exclusions may be a result of two (not exclusive) factors; the presence or absence of predators, and larval responses to two different physical regimes. These alternatives have rarely been separated (Choat 1982; Keough 1982b). The above examples have in common the question of how much the observed pattern of recruitment reflects active choices by larvae, and how much it reflects mortality subsequent to settlement. As a consequence, the implicit assumption of many studies is that settlement can be measured with sufficient accuracy by recruitment, i.e. either there is little mortality during the first few weeks after settlement, or the mortality processes affect all species equally, so that their relative abundances are unchanged. Here, we describe the patterns of recruitment for four sessile invertebrate taxa and estimate mortality rates for those taxa during the first three to four weeks after settlement. The four taxa are Spirorbis eximus (Polychaeta: Serpulidae), and the bryozoans Tubulipora spp. (T. concinna and T. tuba; Cyclostomata: Tubuliporidae) Scrupocellaria bertholetti (Cheilostomata: Scrupocellariidae), and Celleporaria brunnea (Cheilostomata: Celliporidae). Predation by fishes is an important source of mortality of sessile organisms in the study area (Downes& Keough unpubl, obs.), of which the most important fish species are the garibaldi, Hypsypops rubicundus (Pomacentridae), the rock wrasse, HaIichoeres semicinetus (Labridae), and juvenile black surfperch, Embioticajacksoni (Embiotocidae). The sessile organisms live attached to hard substrata, inter alia vertical rock faces. These rock surfaces are uneven, and often bear small pits and cracks, which may offer protection for settling larvae since they are inaccessible to fish. Our aim was to measure the extent to which such refuges are used by recruits, and to separate the presence of active choice by settling larvae from subsequent mortality to yield observed patterns of recruitment. There are a number of ways in which larvae may respond to the presence of such refuges, and in the absence of in situ observations of the behaviour of the larvae, inferences about such responses can be made only from the spatial distribution of juveniles, more specifically the proportion of juveniles that occur in refuges, relative to the number on more exposed surfaces. A number of models of larval behaviour can be erected that predict different spatial patterns: 1. No searching (Dropped-egg model.) Larvae encounter a substratum, but only test it for suitability, and do not search extensively over the substratum. The predicted pattern: Recruits are distributed in refuges and on exposed surfaces in proportion to the surface areas of substratum in the plane of the substratum surface. In this study, the ratio of cross-sectional surface area of refuges to exposed surfaces was 2 : 98. 2. Searching, but no active choice (Ping-pong ball model). Larvae encounter a substratum, and search over it, but settle at random on any surface that is suitable, i.e. no choice of microhabitats. The predicted pattern : Recruits are distributed in proportion to the total surface area of refuges, compared to exposed surfaces. In this case, the ratio is 8:92. 3. Searching and active choice of microhabitat. Larvae encounter the substratum, search over it, and then select microhabitats (refuges) for settlement. The predicted pattern." Recruits are found disproportionately in refuges. In this case, the ratio exceeds 8:92. Methods The study site was characterised by north-east facing vertical rock faces beneath a canopy of Macro cystis pyrifera at Isthmus Reef, approximately 500 m from the Catalina Marine Science Center on Santa Catalina Island in southern California (33~ 118~ Experimental substrata were 150 m m • 150 m m unglazed clay tiles, chosen for their similarity in colour and texture to natural rock surfaces in the area. They were mounted flush against vertical faces at a depth of about 10 m. Refuges from fish were provided on plate surfaces by drilling small pits, 5 mm in diameter and 5 m m deep, on the exposed face of each tile. Twenty randomly positioned pits were drilled on each tile. Surfaces of tlhe panels are thus termed either "pits ", or "flats". Fish were excluded from half of the panels by placing small cages over each experimental panel. The cages were made from 1.5-2 m m diameter plastic-coated wire, with mesh sizes 65 r a m • ram. Previous observations suggested that fish avoided these meshes, and we have never observed any fish feeding through the meshes. Panels were placed at three experimental "sites", about 3-5 m from each other. The experiment was done twice, in November and December 1981. Both caged and uncaged panels were placed at each site. In November, each combination of treatment and site was replicated once, whilst two replicates were used in December. The experiment thus had three factors, caging, site, and time, and was analysed by analysis of variance. Spatial patterns of recruits were examined by testing the observed patterns against the predictions made by the three models of larval behaviour by log-likelihood ratio goodness-of-fit test (Bishop et al. 1975). Results "Settlement" - Distribution of Recruits in the Absence ofFish The distribution of juvenile Tubulipora on caged panels was consistent with the non-searching (dropped-egg) model, while that for Spirorbis differed from the pattern predicted by this model. The distributions of both Spirorbis and Tubulipora were in accord with models that do not invoke selection of microhabitats (Table 1). Scrupocellaria and Celleporaria both showed patterns of recruitment on caged panels that differed from both of the first two models (Table 1), with disproportion ately more recruits in the pits. This was especially so for ScrupoceIlaria, where 88% of recruits were found in the pits. Recruitment - Distribution of Recruits in the Presence ofFish Again, TubuIipora and Spirorbis showed patterns of recruitment that were consistent with the null hypothesis of no selection of microhabitats (Table 1), but in this case, the 350 Table 1. Distribution of recruits in pits and on flat surfaces of caged (C) and uncaged (U) panels. Data were pooled across all times and sites. Three G statistics are shown. All are log-likelihood ratio tests with df= 1. (1)Goodness-of-fit of observed distribution to an expected ratio of 2: 98 (H 1: Ratio > 2: 98). (2) Goodness-of-fit of observed distribution to an expected ratio of 8 : 92 (H 1: Ratio > 8 : 92). (3) Test of independence of the spatial distribution of recruits on caged and uncaged panels (2 • 2 contingency table). The models that generate the expected spatial distributions of recruits are described on P-2. n s = P > 0 . 0 5 ; * P<0.05; ** P<0.01 ; *** P<0.00t Spirorbis Tubulipora spp. Scrupocellaria Celleporaria C U C U C U C U Pits Flat surfaces 47 967 47 820 20 811 22 311 66 9 26 2 20 109 10 61 (1) Goodness-of-fit G (2) Goodness-of-fit G (3) Independence G 26.3*** 35.5*** 22.6*** 460*** 189"** 49.6*** 23.0*** 18.2 ns 8.8 ns 0.9 ns 280*** 117"** 7.9** 3.0* 0.66 ns 47.7*** 0.61 ns Table 2, Analyses of variance for the effects of time, site, and caging on the numbers of recruits on the exposed surfaces of panels, n s = P > 0 . 0 5 ; * P<0.05; ** P<0.01 10.85" Source of variation df Caging Site Times CxS CxT SxT CxSxT Residual 1 2 1 2 1 2 2 6 Table 3. Means and standard deviations (in parentheses) of the number of recruits per panel for caged and uncaged panels at three sites. Data were pooled across time periods, and only recruits on flat surfaces are included, n = 3 in all cases Taxon Site Caged Uncaged Spirorbis 1 2 3 178 (22) 87 (88) 8 (6) 131 (58) 80 (60) 29 (33) Tubulipora 1 2 3 34 (16) 223 (26) 116 (54) 15 (9) 92 (77) 62 (55) Scrupocellaria 1 2 3 2.3 (1.5) 0.3 (0.6) 0.3 (0.6) 0 0.7 (1.2) 0 Celleporaria 1 2 3 12 (8) 12 (7) 5 (4) 4 (3) 9 (9) 5 (4) distribution of Tubulipora recruits differed significantly from the predictions of the no-searching (dropped-egg) model, but was in accordance with the second (ping-pong ball) model. The distribution of Spirorbis recruits was unchanged. Celleporaria and Scrupoeellaria were still found disproportionately more often in the pits (Table 1). 0.13 ns Spirorbis 0.07 ns Tubulipora Celleporaria MS F MS F MS F 567 28,108 2,434 1,734 1,320 728 7,405 2,138 0.27 ns 13.14"* 1.14 ns 0.81 ns 0.62 ns 0.34 ns 3.46 ns 20,808 26,274 7,168 4,925 256 3,618 522 1,698 12.25" 15.47'* 4.22 ns 2.90 ns 0.15 ns 2.13 ns 0.3i ns 46.7 43.5 103.4 20.2 34.0 8.4 7.5 55.3 0.85 ns 0.79 ns 1.87 ns 0.37 ns 0.62 ns 0.15 ns 0.14 ns Effects offish on the Abundance of Recruits The survival rate of juveniles was assessed by comparing the n u m b e r of recruits on flat surfaces of caged and uncaged panels. It is unlikely that the cages used have major effects on recruitment, but this was checked by comparing the n u m b e r of recruits in pits, since they are protected from predation by fish whether in cages or not. The n u m b e r of Spirorbis recruits per panel did not differ between uncaged and caged panels (Table 2), although there was a strong difference between the sites (Tables 2, 3). The n u m b e r of recruits in the pits in the two treatments was almost identical (Table 1). Tubulipora was markedly less a b u n d a n t on uncaged panels (Tables 2, 3), although there was no difference in the n u m b e r in the pits (Table 1). Celleporaria showed no marked difference with caging (Table 2), despite a difference in the n u m b e r of recruits in the pits (Table 1). This was due to a single caged panel in December, which received thirty recruits. There was no difference between the sites for Celleporaria (Table 2). Only two Scrupocellaria recruits were observed on exposed surfaces of uncaged panels, and analysis of variance was not possible. Nine recruits were observed on the caged panels, but this difference is not sufficient to reject the null hypothesis that recruits occur equally frequently on both types of panels (Binomial test, P = 0.065). A more sensitive test of the effect of predation on Scrupocellaria comes from examination of recruits in the pits. Scrupocellaria has an 351 arborescent growth form, and colonies in the pits quickly grow out of the pits, i.e. taller than 5 mm. For the December series of panels, all colonies were categorized as being less than or greater than 5 m m high, i.e. accessible or not accessible to fish. On caged panels, there were 14 "tall" colonies out of 36, while on the uncaged panels, none of the 17 colonies were higher than 5 mm. These distributions are different from each other (log-likelihood ratio test on 2 x 2 contingency table, G=9.06, d f = l , P<0.01). These data suggest that as colonies grow tall, the pits no longer act as refuges, and the colonies may be picked off. Observations in the laboratory showed that when the protruding parts of a colony were pulled, the whole colony was removed, and so the small colonies in the pits of uncaged panels were juvenile colonies rather than remnants of older ones. Thus, the number of juvenile colonies did not differ between the two treatments (22 in caged vs. 17 in uncaged). That is, there was no evidence of differential settlement into caged areas. Although sample sizes were small, neither of the colonies on uncaged exposed surfaces were large, while three of nine on caged panels were large. Discussion The observations on uncaged panels correspond to recruitment as reported in the literature; in fact, the time before first census by us was shorter than in many studies. The relationship between settlement and recruitment is not strong, nor is it constant between species. A few field studies exist that have documented the mortality of juveniles of a single species (Connell 1961; Denley 1981; Goodbody 1965), but these studies have attributed much of the mortality of recruits to physical factors or to competition. These results show that there may also be substantial mortality due to predation. Further, the small, poorly-calcified stages of the four taxa differ in their susceptibility to predation. The observed patterns of early mortality are also likely to vary in time, since reproduction of many invertebrate species is seasonal. The intensity of predation may also vary, both seasonally (e.g. Haldorsen and Moser 1979), or with age of fish (S. Holbrook and R. Schmitt, personal communication). Similar changes in foraging behaviour are known for invertebrate predators (Keough and Butler 1979; Menge 1972; Paine 1969). The processes shown here operate on time scales shorter than the interval between censuses in many studies of predation (e.g. Day 1977; Day and Osman 1982; Keough and Butler 1979; Russ 1980; Sammarco 1980). The actual response of larvae to cages has not been investigated, and it is therefore possible that apparent effects, or lack of effects could be due not only to the exclusion of predators, but also to a complex interaction between larval behaviour and predation that occurs before the first census by an observer. Inferring Larval Behaviour The observed patterns of recruitment can be classified as suggesting no selection of microhabitats (Spirorbis, Tubulipora), or suggesting varying degrees of active selection of microhabitats. Juveniles may suffer extensive mortality during the first weeks after settlement. Predation may alter the abundance (Tubulipora), spatial distribution (Tubulipora), or size distribution of the population of juvenile or- ganisms (Scrupocellaria). Alternatively, species may be relatively unaffected by predation (Celleporaria, Spirorbis). The susceptibility to predation by fish is thus not clearly related to the inferred behaviour of larvae, since of the species that are affected by predation, one shows strong selection of microhabitats, while the other settles apparently at random. A similar pattern is seen for species not affected by predation. Direct observations of larvae often can not be made, and the decisions made by larvae must be inferred from the distribution of juveniles. Such inferences are usually made from exposed substrata, and thus may be misleading. For Tubulipora, such observations of recruitment would support the second (ping-pong ball) model, and would lead to the rejection of the no-searching (dropped-egg) modeI. If the effect of fish is removed, the reverse is true, and the data suggest that Tubulipora larvae settle as they encounter suitable substrata. In sum, the period immediately following settlement and metamorphosis of sessile marine invertebrates may involve heavy mortality, so that variation in recruitment naay be due to a combination of planktonic events, active choices by larvae, and subsequent mortality. Inferences about causes of distributions of adult organisms or of patterns of community structure that are based on observations of recruitment may be erroneous, since they can not distinguish between these sources of variation. From the viewpoint of management of commercial populations of marine invertebrates, the distinction is important, since a major component due to mortality of juveniles is amenable to experimental modification, while variations that are derived from events in the plankton are much less manipulable. Acknowledgements. We are grateful to R. Schmitt, A. Butler, S. Holbrook, and S. Swarbrick for their helpful discussions and for their comments on the manuscript. We also thank Dr. R. 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