Recruitment of Marine Invertebrates: the Role of Active Larval Choices and Early Mortality

Home , Marine invertebrates, Recruitment (biology)

Oecologia (Berl) (1982) 54:348-352 Oer Springer-Verlag 1982

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 a reflection of the limitations of the observer. The number marine invertebrates with planktonic larvae may be derived of organisms passing through the fourth phase is termed from a number of sources: events within the plankton, recruitment, while the number passing to the third phase choices made by larvae at the time of settlement, and mor- is termed settlement. Recruitment is a composite of larval tality of juvenile organisms after settlement, but before a and juvenile stages, while settlement involves only larval census by an observer. These sources usually are not distin- stages. guished. It is important to distinguish between settlement and A study of the recruitment of four species of sessile recruitment. Non-random patterns of recruitment, such as invertebrates living on rock walls beneath a kelp canopy differences in the density of recruitment with height on the showed that both selection of microhabitats by settling shore (Underwood 1979) or differences in the density of larvae and predation by fish may be important. Two micro- recruitment with patch size (Jackson 1977; Keough 1982a), habitats were of interest; open, flat rock surfaces, and small or with microhabitat, may have two causes: (1) differential pits and crevices that act as refuges from fish predators. settlement, and (2), different probabilities of early mortality The polychaete Spirorbis eximus and the cyclostome in different parts of an organism's habitat. The first may bryozoan Tubulipora spp. showed no preference for refuges , involve an active response by larvae at the time of settle- but settled apparently at random on the available substrata. ment that may be an evolved response to patterns of mortal- Tubulipora was preyed upon heavily by fish, while Spiro~rbis ity, while the second involves no active choice by larvae. was relatively unaffected. The bryozoans Celleporaria Failure to distinguish between these two phenomena brunnea and Scrupocellaria bertholetti both recruited prefer- may lead to misleading inferences in a number of areas. entially into refuges. Scrupocellaria were preyed upon, while First, explanations for the spatial distributions of adult or- Celleporaria juveniles seemed unaffected. Predation by fish ganisms have frequently neglected the importance of re- modified the spatial distribution (Tubulipora), abundance cruitment (Underwood and Denley 1982), and second, (Tubulipora), or size distribution (Scrupocellaria) of the ju- many of the studies that have included recruitment in the venile population, or had relatively little effect (Cellepor- interdidal zone of rocky shores, have not distinguished be- aria, Spirorbis). tween recruitment and settlement. This may have led to All of the above events occur within three weeks of an overestimation of the importance of interactions between settlement. Since inferences about the effect of larval events adult organisms and physical factors in limiting these distri- on the population dynamics of adult organisms are often butions. The same is true of work on subtidal hard sub- based on observations of the patterns of recruitment after strata; the terms recruitment and settlement are used inter- one or two months, they are therefore likely to be mislead- changeably, when recruitment is actually measured. Pat- ing. terns 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; Introduction. Schoener and Schoener 1981). At the community level, it has been suggested for some The colonisation of habitats by marine organisms with subtidal systems, species arriving first may be able to resist planktonic larvae involves three phases: development (in- further invasion by other species, so that the abundance cluding dispersal as a planktonic form), testing of a habitat of sessile species in such communities can be explained by for suitability, and settlement (summarised by Underwood measuring the colonising ability of component species (e.g. 1979). For sessile invertebrates, the latter phase also in- Dean and Hurd 1980; Sutherland and Karlson 1977). It cludes attachment to the substratum and metamorphosis. is often considered that the ability of a species to colonise The organism is unlikely to be detected immediately, be- a habitat can be measured accurately by its recruitment cause of small size, cryptic habitat, etc., and there is a fourth rate (usually over a time period of 1-2 mo.). "phase", survival until the organisms is counted by an In a similar way, many other studies have considered observer. This phase may last from hours to months (Schel- the effect of predation in natural communities (e.g. Day tema 1974), but it is not a true life-history stage, merely 1977; Day and Osman 1982; Keough and Butler 1979; Offprint requests to." M.J. Keough Osman 1977; Paine 1966; Russ 1980; Sammarco 1980).

0029-8549/82/0054/0348/$01.00 349

Most have used exclusions (cages, fences, etc.) that modify 3. Searching and active choice of microhabitat. Larvae the physical environment, such as light, water flow, sedi- encounter the substratum, search over it, and then select mentation, in some way. Differences in the abundance of microhabitats (refuges) for settlement. The predicted taxa between controls and exclusions may be a result of pattern." Recruits are found disproportionately in refuges. two (not exclusive) factors; the presence or absence of pre- In this case, the ratio exceeds 8:92. dators, and larval responses to two different physical re- gimes. These alternatives have rarely been separated (Choat Methods 1982; Keough 1982b). The above examples have in common the question of The study site was characterised by north-east facing verti- how much the observed pattern of recruitment reflects cal rock faces beneath a canopy of Macro cystis pyrifera active choices by larvae, and how much it reflects mortality at Isthmus Reef, approximately 500 m from the Catalina subsequent to settlement. As a consequence, the implicit Marine Science Center on Santa Catalina Island in southern assumption of many studies is that settlement can be mea- California (33~ 118~ sured with sufficient accuracy by recruitment, i.e. either Experimental substrata were 150 mm• 150 mm un- there is little mortality during the first few weeks after settle- glazed clay tiles, chosen for their similarity in colour and ment, or the mortality processes affect all species equally, texture to natural rock surfaces in the area. They were so that their relative abundances are unchanged. mounted flush against vertical faces at a depth of about Here, we describe the patterns of recruitment for four 10 m. Refuges from fish were provided on plate surfaces sessile invertebrate taxa and estimate mortality rates for by drilling small pits, 5 mm in diameter and 5 mm deep, those taxa during the first three to four weeks after settle- on the exposed face of each tile. Twenty randomly posi- ment. tioned pits were drilled on each tile. Surfaces of tlhe panels The four taxa are Spirorbis eximus (Polychaeta: Serpuli- are thus termed either "pits ", or "flats". dae), and the bryozoans Tubulipora spp. (T. concinna and Fish were excluded from half of the panels by placing T. tuba; Cyclostomata: Tubuliporidae) Scrupocellaria small cages over each experimental panel. The cages were bertholetti (Cheilostomata: Scrupocellariidae), and Celle- made from 1.5-2 mm diameter plastic-coated wire, with poraria brunnea (Cheilostomata: Celliporidae). Predation mesh sizes 65 ram• ram. Previous observations sug- by fishes is an important source of mortality of sessile or- gested that fish avoided these meshes, and we have never ganisms in the study area (Downes& Keough unpubl, obs.), observed any fish feeding through the meshes. of which the most important fish species are the garibaldi, Panels were placed at three experimental "sites", about Hypsypops rubicundus (Pomacentridae), the rock wrasse, 3-5 m from each other. The experiment was done twice, HaIichoeres semicinetus (Labridae), and juvenile black surf- in November and December 1981. Both caged and uncaged perch, Embioticajacksoni (Embiotocidae). panels were placed at each site. In November, each combi- The sessile organisms live attached to hard substrata, nation of treatment and site was replicated once, whilst inter alia vertical rock faces. These rock surfaces are uneven, two replicates were used in December. The experiment thus and often bear small pits and cracks, which may offer pro- had three factors, caging, site, and time, and was analysed tection for settling larvae since they are inaccessible to fish. by analysis of variance. Our aim was to measure the extent to which such refuges Spatial patterns of recruits were examined by testing are used by recruits, and to separate the presence of active the observed patterns against the predictions made by the choice by settling larvae from subsequent mortality to yield three models of larval behaviour by log-likelihood ratio observed patterns of recruitment. goodness-of-fit test (Bishop et al. 1975). There are a number of ways in which larvae may respond to the presence of such refuges, and in the absence Results of in situ observations of the behaviour of the larvae, inferences about such responses can be made only from the "Settlement" - Distribution of Recruits spatial distribution of juveniles, more specifically the pro- in the Absence ofFish portion of juveniles that occur in refuges, relative to the number on more exposed surfaces. A number of models The distribution of juvenile Tubulipora on caged panels was of larval behaviour can be erected that predict different consistent with the non-searching (dropped-egg) model, spatial patterns: while that for Spirorbis differed from the pattern predicted 1. No searching (Dropped-egg model.) Larvae encounter by this model. The distributions of both Spirorbis and Tubu- a substratum, but only test it for suitability, and do not lipora were in accord with models that do not invoke selec- search extensively over the substratum. The predicted tion of microhabitats (Table 1). pattern: Recruits are distributed in refuges and on exposed Scrupocellaria and Celleporaria both showed patterns surfaces in proportion to the surface areas of substratum of recruitment on caged panels that differed from both of in the plane of the substratum surface. In this study, the the first two models (Table 1), with disproportion ately more ratio of cross-sectional surface area of refuges to exposed recruits in the pits. This was especially so for ScrupoceIlaria, surfaces was 2 : 98. where 88% of recruits were found in the pits. 2. Searching, but no active choice (Ping-pong ball model). Larvae encounter a substratum, and search over it, but Recruitment - Distribution of Recruits settle at random on any surface that is suitable, i.e. no in the Presence ofFish choice of microhabitats. The predicted pattern : Recruits are distributed in proportion to the total surface area of ref- Again, TubuIipora and Spirorbis showed patterns of recruit- uges, compared to exposed surfaces. In this case, the ratio ment that were consistent with the null hypothesis of no is 8:92. 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. ns=P>0.05; * P<0.05; ** P<0.01 ; *** P<0.00t

Spirorbis Tubulipora spp. Scrupocellaria Celleporaria

C U C U C U C U

Pits 47 47 20 22 66 26 20 10 Flat surfaces 967 820 811 311 9 2 109 61

(1) Goodness-of-fit 26.3*** 35.5*** 0.66 ns 22.6*** 460*** 189"** 49.6*** 23.0*** G (2) Goodness-of-fit 18.2 ns 8.8 ns 47.7*** 0.9 ns 280*** 117"** 7.9** 3.0* G (3) Independence 0.61 ns 10.85" 0.13 ns 0.07 ns G

Table 2, Analyses of variance for the effects of time, site, and caging Source df Spirorbis Tubulipora Celleporaria on the numbers of recruits on the exposed of surfaces of panels, variation MS F MS F MS F ns=P>0.05; * P<0.05; ** P<0.01 Caging 1 567 0.27 ns 20,808 12.25" 46.7 0.85 ns Site 2 28,108 13.14"* 26,274 15.47'* 43.5 0.79 ns Times 1 2,434 1.14 ns 7,168 4.22 ns 103.4 1.87 ns C x S 2 1,734 0.81 ns 4,925 2.90 ns 20.2 0.37 ns C x T 1 1,320 0.62 ns 256 0.15 ns 34.0 0.62 ns SxT 2 728 0.34 ns 3,618 2.13 ns 8.4 0.15 ns CxSxT 2 7,405 3.46 ns 522 0.3i ns 7.5 0.14 ns Residual 6 2,138 1,698 55.3

Table 3. Means and standard deviations (in parentheses) of the Effects offish on the Abundance of Recruits number of recruits per panel for caged and uncaged panels at three sites. Data were pooled across time periods, and only recruits The survival rate of juveniles was assessed by comparing on flat surfaces are included, n = 3 in all cases the number of recruits on flat surfaces of caged and uncaged panels. It is unlikely that the cages used have major effects Taxon Site Caged Uncaged on recruitment, but this was checked by comparing the number of recruits in pits, since they are protected from Spirorbis 1 178 (22) 131 (58) 2 87 (88) 80 (60) predation by fish whether in cages or not. 3 8 (6) 29 (33) The number of Spirorbis recruits per panel did not differ between uncaged and caged panels (Table 2), although 1 34 (16) 15 (9) Tubulipora there was a strong difference between the sites (Tables 2, 2 223 (26) 92 (77) 3 116 (54) 62 (55) 3). The number of recruits in the pits in the two treatments was almost identical (Table 1). Tubulipora was markedly Scrupocellaria 1 2.3 (1.5) 0 less abundant on uncaged panels (Tables 2, 3), although 2 0.3 (0.6) 0.7 (1.2) there was no difference in the number in the pits (Table 1). 3 0.3 (0.6) 0 Celleporaria showed no marked difference with caging (Ta- Celleporaria 1 12 (8) 4 (3) ble 2), despite a difference in the number of recruits in the 2 12 (7) 9 (9) pits (Table 1). This was due to a single caged panel in De- 3 5 (4) 5 (4) cember, which received thirty recruits. There was no difference between the sites for Celleporaria (Table 2). Only two Scrupocellaria recruits were observed on ex- distribution of Tubulipora recruits differed significantly posed surfaces of uncaged panels, and analysis of variance from the predictions of the no-searching (dropped-egg) was not possible. Nine recruits were observed on the caged model, but was in accordance with the second (ping-pong panels, but this difference is not sufficient to reject the null ball) model. The distribution of Spirorbis recruits was un- hypothesis that recruits occur equally frequently on both changed. types of panels (Binomial test, P= 0.065). A more sensitive Celleporaria and Scrupoeellaria were still found dispro- test of the effect of predation on Scrupocellaria comes from portionately more often in the pits (Table 1). examination of recruits in the pits. Scrupocellaria has an 351 arborescent growth form, and colonies in the pits quickly ganisms (Scrupocellaria). Alternatively, species may be rela- grow out of the pits, i.e. taller than 5 mm. For the De- tively unaffected by predation (Celleporaria, Spirorbis). The cember series of panels, all colonies were categorized as susceptibility to predation by fish is thus not clearly related being less than or greater than 5 mm high, i.e. accessible to the inferred behaviour of larvae, since of the species or not accessible to fish. On caged panels, there were 14 that are affected by predation, one shows strong selection "tall" colonies out of 36, while on the uncaged panels, of microhabitats, while the other settles apparently at none of the 17 colonies were higher than 5 mm. These distri- random. A similar pattern is seen for species not affected butions are different from each other (log-likelihood ratio by predation. test on 2 x 2 contingency table, G=9.06, df=l, P<0.01). Direct observations of larvae often can not be made, These data suggest that as colonies grow tall, the pits no and the decisions made by larvae must be inferred from longer act as refuges, and the colonies may be picked off. the distribution of juveniles. Such inferences are usually Observations in the laboratory showed that when the pro- made from exposed substrata, and thus may be misleading. truding parts of a colony were pulled, the whole colony For Tubulipora, such observations of recruitment would was removed, and so the small colonies in the pits of support the second (ping-pong ball) model, and would lead uncaged panels were juvenile colonies rather than remnants to the rejection of the no-searching (dropped-egg) modeI. of older ones. Thus, the number of juvenile colonies did If the effect of fish is removed, the reverse is true, and not differ between the two treatments (22 in caged vs. 17 the data suggest that Tubulipora larvae settle as they en- in uncaged). That is, there was no evidence of differential counter suitable substrata. settlement into caged areas. Although sample sizes were In sum, the period immediately following settlement and small, neither of the colonies on uncaged exposed surfaces metamorphosis of sessile marine invertebrates may involve were large, while three of nine on caged panels were large. heavy mortality, so that variation in recruitment naay be due to a combination of planktonic events, active choices Discussion by larvae, and subsequent mortality. Inferences about causes of distributions of adult organisms or of patterns The observations on uncaged panels correspond to recruit- of community structure that are based on observations of ment as reported in the literature; in fact, the time before recruitment may be erroneous, since they can not distin- first census by us was shorter than in many studies. The guish between these sources of variation. From the view- relationship between settlement and recruitment is not point of management of commercial populations of marine strong, nor is it constant between species. A few field studies invertebrates, the distinction is important, since a major exist that have documented the mortality of juveniles of component due to mortality of juveniles is amenable to a single species (Connell 1961; Denley 1981; Goodbody experimental modification, while variations that are derived 1965), but these studies have attributed much of the mortal- from events in the plankton are much less manipulable. ity of recruits to physical factors or to competition. These results show that there may also be substantial mortality Acknowledgements. We are grateful to R. Schmitt, A. Butler, S. due to predation. Further, the small, poorly-calcified stages Holbrook, and S. Swarbrick for their helpful discussions and for of the four taxa differ in their susceptibility to predation. their comments on the manuscript. We also thank Dr. R. Given The observed patterns of early mortality are also likely to for his help, and permission to use the facilities at Catalina Manne Science Center. vary in time, since reproduction of many invertebrate This is publication number 68 from the Catalina Marine species is seasonal. The intensity of predation may also Science Center. vary, both seasonally (e.g. Haldorsen and Moser 1979), or Financial support to M.J.K. was provided by an NSF grant with age of fish (S. Holbrook and R. Schmitt, personal to J.H. Connell. communication). Similar changes in foraging behaviour are known for invertebrate predators (Keough and Butler 1979; Menge 1972; Paine 1969). References The processes shown here operate on time scales shorter Choat JH (1982) The influence of fish predation on benthic com- than the interval between censuses in many studies of preda- munities. Ms tion (e.g. Day 1977; Day and Osman 1982; Keough and Connell JH (1961) Effect of competition, predation by Thais lapil- Butler 1979; Russ 1980; Sammarco 1980). The actual re- lus, and other factors on natural populations of the barnacle, sponse of larvae to cages has not been investigated, and Balanus balanoides. Ecol Monogr 31:61 104 it is therefore possible that apparent effects, or lack of Day RW (1977) Two contrasting effects of predation on species effects could be due not only to the exclusion of predators, richness in coral reef habitats. Mar Biol 44:1-5 but also to a complex interaction between larval behaviour Day RW, Osman RW (1982) Predation by Patiria miniata (Asteroi- dea) on bryozoans: prey diversity may depend on the mecha- and predation that occurs before the first census by an nism of succession. Oecologia (Berl.) 51 : 300-309 observer. Dean TA, Hurd LE (1980) Development in an estuarine fouling community: the influence of early colonists on later arrivals. Inferring Larval Behaviour Oecologia (Berl) 45:295-301 Denley EJ (1981) The ecology of the intertidal barnacle, Tessero- The observed patterns of recruitment can be classified as pera rosea. PhD thesis, University of Sydney, Australia suggesting no selection of microhabitats (Spirorbis, Tubuli- Goodbody I (1965) The biology of Ascidia nigra (Savigny). III The pora), or suggesting varying degrees of active selection of annual pattern of colonization. Biol Bull 129:128-133 Haldorsen L, Moser M (1979) Geographic patterns of prey utiliza- microhabitats. Juveniles may suffer extensive mortality dur- tion in two species of surfperch (Embiotocidae) Copeia ing the first weeks after settlement. Predation may alter 1979 : 567-572 the abundance (Tubulipora), spatial distribution (Tubuli- Jackson JBC (1977) Habitat area, colonization and development pora), or size distribution of the population of juvenile or- of epibenthic community structure. In" BF Keegan, PO Ceidigh 352

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