Marine Biology

, Volume 145, Issue 1, pp 201–214

Temporal and spatial components of variability in benthic recruitment, a 5-year temperate example

Authors

    • Department of Zoology, Ecology and Plant SciencesNational University of Ireland
  • D. K. A. Barnes
    • British Antarctic SurveyNERC
Research Article

DOI: 10.1007/s00227-003-1291-5

Cite this article as:
Watson, D.I. & Barnes, D.K.A. Marine Biology (2004) 145: 201. doi:10.1007/s00227-003-1291-5

Abstract

Deployment of artificial substrata is a common method of investigating early community development and recruitment, but rarely are such experiments of long enough duration to include even year time scales. We placed replicate, machined-slate panels (15×15 cm) in the intertidal and at depths of 6 and 12 m at two sites of differing flow rate at Lough Hyne, SW Ireland. These were serially replaced every 30–60 days for a period of 5 years (1997–2002), except in the intertidal (2000–2002). The number and identity of all recruits were recorded. Recruitment varied over several orders of magnitude both on temporal and spatial scales. The greatest source of variability was between the intertidal (with few species or recruit numbers) and the subtidal zones (many species, some with thousands of recruits per panel per 30 days). Highest levels of recruitment occurred at the low-flow site (Labhra Cliff). Here, recruitment was dominated by the serpulid polychaete, Pomatoceros sp., reaching ~4000 individuals per panel per 30 days. Highest species richness occurred, however, at the high flow site (Whirlpool Cliff). At this site more colonial forms (e.g. bryozoans) settled. Season was found to be the dominant pattern explaining subtidal recruit and species number variability. Year, however, was the dominant temporal pattern explaining change in diversity (Shannon–Wiener H′). In space, depth explained most variability of recruit numbers, whereas site explained more variation in species richness. Both these spatial factors contributed similarly to variability of diversity (H′). Recruitment has long been known to vary considerably over large spatial scales, such as with latitude and isolation, but we that show changes of a similar magnitude in recruitment can occur across small spatial scales. Individual taxa showed varied temporal patterns of recruitment including continuous, regular seasonal fluctuations and irregular pulses in particular years.

Introduction

Many marine invertebrates have limited powers of movement as adults; indeed, all representatives of some higher taxa are sessile. For species with such sessile or sedentary adults, gametes, fertilised eggs, larvae and/or juveniles potentially have an important function as a dispersal stage. The size, sometimes shape and often provision of self-contained nutrition may allow these various sub-adult stages possibilities of wide passive transport in air or water currents (Scheltema 1971, 1986). The last few decades have seen a return of the focus from adult processes to “supply-side” ecology in attempts to define patterns of marine benthic community dynamics (Underwood and Fairweather 1989). Clearly, only once larvae have successfully recruited can adult processes even begin to have an influence, so an understanding of recruitment and pre-recruitment scales, patterns and influences is likely to be important in the interpretation of the “big picture” (Menge 1991; Rodrigues et al. 1993). Propagules of marine benthic animals vary enormously in their timing, and the larvae differ in mode, durability, nutritional status and settlement behaviour. Broadly, larval types vary between three extremes: brooded, lecithotrophic and planktotrophic. Many of these types offer relatively short-distance transport, because of restricted duration of viability, but some planktotrophic larvae may be capable of travel over thousands of kilometres (Scheltema 1971, 1986). Trans-oceanic opportunities are offered by recruitment of larvae onto flotsam such as pumice, plant propagules, floating shells or kelp (Guppy 1889; Richards 1958) or, more recently, using anthropogenic constructions such as ships (Carlton and Hodder 1995) and marine debris (Barnes 2002).

Two different methods for examining recruitment of marine benthos have emerged: use of natural or artificial substrata. The advantages of using machined panels are multi-fold, but the main reason is the possibility of minimising surface heterogeneity. Firstly, study areas can be of similar size and shape, so replication can be increased; secondly, study areas are flat, which facilitates locating and identifying recruits; and, thirdly, study areas can easily be manipulated to examine particular factors such as region (Schoener et al. 1978), locality (Todd and Turner 1986), light (Nandakumar 1995), depth (Barnes 1996), latitude and isolation (Holmes et al. 1997) and sediment load (Maughan 2001). One shortcoming of many such studies is the time scale used. Although Dayton (1989) reported on recruitment to polar panels during a 10-year study, he only examined panels on sporadic occasions and even then only once in sufficient detail to reveal new microscopic recruits. Typically the longer time scales for which recruitment of marine benthos to artificial (or natural) substrata have been studied are 2–3 years (Maturo 1959; Chalmer 1982; Pisano and Boyer 1985; Todd and Turner 1986; Menge 1991; Relini et al. 1994; Maughan 2000). This clearly makes meaningful analysis of inter-annual patterns of variability difficult. The extensive literature pertaining to recruitment variability in broadcast-spawning fishes has shown such inter-annual, and indeed inter-decadal, patterns to exist (Rothschild 2000). It has been theorised that such patterns are related to oceanic-scale hydrographic patterns (Corten 1990).

Southward (1980), amongst others, has repeatedly emphasised the importance of “long-term” studies in all aspects of ecology, and patterns on greater than annual scales are well known (Moran 1986; Dayton 1989; Elner and Vadas 1990; Planque and Fox 1998). Particular localities, usually adjacent to the sites of marine laboratories, have now accrued observations of physical and biological parameters over many decades. Lough Hyne, a semi-enclosed sea lough in SW Ireland, has, in particular, been a centre for inter-linked studies, organism monitoring and population census efforts since the late 1920s. Some of the most common and abundant marine benthic organisms at Lough Hyne exhibit recruitment phases on longer than annual scales (Barnes et al. 2002). Although studies of larvae in the plankton at Lough Hyne commenced more than a decade ago (Minchin 1992), investigations of invertebrate recruitment, other than barnacles (O’Riordan et al. 1992), did not begin until 1997. Here, we describe scales and patterns of marine benthos recruitment to artificial panels over a 5-year period. Recruitment was defined as in Stanwell-Smith and Barnes (1997), which is “organisms that settled onto the panels had metamorphosed, thus making the beginnings of their sessile life”. We tested the hypothesis that no scale in either time (month, season or year) or space (within site replicates, between sites or depths) dominates the pattern of recruitment.

Materials and methods

Artificial substrata, in the form of machined-slate panels, were serially replaced every 30–60 days over a 5-year period at two sites at Lough Hyne, SW Ireland (51°31′N; 9°10′W). Lough Hyne is a small (0.8×0.6 km) sea lough linked to the Atlantic Ocean by a narrow (>20 m wide) channel, known as the “Rapids”. The salinity and temperature regimes are similar to those in the adjacent coastal Atlantic. Temperature readings were taken using continuously logged probes from four sites in the lough, at ~3 m depth. These temperature readings rose to a maximum of ~17°C in August and fell to a minimum of ~7°C in January. The shallow, and narrow, nature of the “Rapids” results in asymmetrical timing of inflow and outflow regimes and a reduced tidal range compared with the Atlantic coastline. The water flow rate through this channel can reach 2–3 m s−1 on both incoming and outgoing tides. Complete exchange of water in the lough with “new” water takes approximately 22 tidal cycles (Kitching and Ebling 1967). As there is bi-directional water exchange along this channel, it can be expected that there is also a bi-directional exchange of larvae between the lough and the Atlantic Ocean, but the recruitment success of these larvae may vary. The surface and subsurface water flow speed and directionality have been described in some detail for Lough Hyne (Bassindale et al. 1948, 1957; Maughan 2000; Bell and Barnes 2002).

Panel replicates were placed at 6 and 12 m depths at the two sites, Whirlpool Cliff and Labhra Cliff (Fig. 1), in October 1997. These sites differ with respect to water flow and related features (water residence time, sedimentation and sediment accumulation rates). The Whirlpool Cliff site, being close to the exchange channel (the “Rapids”), is subject to high flow rates (up to 2 m s−1) on the incoming tide (Bell and Barnes 2002), though not on outgoing tides. Labhra Cliff, further from the point of Atlantic water exchange, has flow rates <5 cm s−1 at all stages of the tidal cycle (Bell 2001). The benthic communities at both Labhra Cliff and Whirlpool Cliff were broadly similar (Picton 1991; Turner and Warman 1991; Maughan and Barnes 2000a; Bell and Barnes 2002). The subtidal panels were changed, every 30–60 days, from October 1997 to September 2002 at all sites/depths. In spring 2000 additional panels were placed in the intertidal (ELWS) at both sites and replaced as with the subtidal panels.
Fig. 1

Map of Lough Hyne, SW Ireland, showing both sites used in this study and the bi-directional channel, known as the “Rapids”, linking the lough with the Atlantic Ocean

The artificial substrata (panels) used in this study followed the design of Todd and Turner (1986). These were machined natural slate panels, each 15 cm×15 cm in size, and attached, in sets of three, to two-angle steel or aluminium bars by plastic cable-ties. A square (10×10 cm) was drawn at the centre of each of the panels using a blue, permanent marker pen; the purpose of this blue background was to facilitate viewing of small or transparent recruits. Drying the blue ink, then soaking them in seawater for 24 h, seasoned the panels. They were subsequently dried again and finally deployed. These “arrays” were then placed, surface down, onto quadrats at each depth. The quadrats enabled all panels to be maintained 2 cm above the substratum. Numbers of benthic recruits were standardised to 30 days to make the periods of immersion of all panels comparable. Our definition of “season” was as in normal usage following Maughan’s (2000) findings that underlying recruitment patterns clustered to season under such a definition. Much work has been focussed on the timing of settlement onto new substrates and the need for the substrates to be “prepared” in some way, namely the need for biofilms. Roberts et al. (1991), however, showed that permanent attachment could occur after only 1 h of immersion of the experimental substratum. Barkai and Branch (1988) showed a peak of species present after 2 months, but most similar studies have sampled monthly (Maturo 1959; Sutherland and Karlson 1977; Chalmer 1982; Menge 1991; Relini et al. 1994; Stanwell-Smith and Barnes 1997). We considered panel replacement each month an appropriate balance between maximising resolution of settling organisms, giving adequate time for recruitment of species present and comparability with other studies.

All colonists were identified to the lowest taxonomic level (mostly species) using Linnean/Field Studies Council and Hayward and Ryland (1995) guides to NW European marine fauna. In some cases taxonomic resolution was restricted due to the size of recruits. Pomatoceros sp. polychaetes, for example, are inseparable morphologically until 8 mm in length (Castric-Fey 1983). Bryozoans, a major component of recruiting fauna, recruit as an initial atypical module “the ancestrula”. From the ancestrula the typical zooids bud, which comprise colonies. Bryozoan colonies occurring as ancestrulae at the time of observation were only separable by taxonomic order or were, in some cases, inseparable. They were thus recorded as “cheilostome ancestrulae”, “cyclostome ancestrulae” or “unidentified bryozoans”. This enabled all recruits to be recorded, even if not to species level. These identification problems, particularly in newly settled organisms, have been encountered in other studies (Todd and Turner 1986).

Homogeneity of variance was tested using Levin’s test. Some, but not all, of the variances within the data collected during this study were heterogeneous, even after log or square root transformation (where appropriate). These departures from homogeneity occur in most/all community metrics, thereby creating restrictions to the use of ANOVA (Rice 2000). Although the transformations did not fully normalise the data, general linear model (GLM) ANOVA tests were chosen, as they are robust to small variations of normality (Zar 1999). Due to this departure from homogeneity, the results of these analyses must be treated with caution, as there is likely to be increased probability of type I error. We have included recruitment patterns of selected taxa at each site and depth as simple two-dimensional kites, for ease of interpretation. We attempted data transformation (log, square root) of this specific taxonomic data to enhance interpretation of patterns, but we considered the results less satisfactory than linear plots.

Results

Variability in recruitment intensity

Individuals of 101 taxa recruited onto the panels between October 1997 and September 2002 (Table 1). Numbers of recruits per 30 days varied over four orders of magnitude in time and space, up to a monthly mean of ~4000 recruits per 10×10 cm panel. The lowest numbers of recruits were typically in the two intertidal sites, whilst the highest were at Labhra 6 m in summer months. Four-factor GLM ANOVA of monthly data from all sites and depths showed both spatial and temporal factors to be highly significant (Table 2) in explaining variability in recruitment. Significant interactions here highlight the fact that absolute recruits at a given depth will vary with season and year. Because of obvious differences between the intertidal and subtidal data (both in terms of length of study period and magnitude of recruitment) and in order to probe the subtidal data in more detail, the analysis was repeated for just the 6 and 12 m data (Table 3). In order of decreasing F statistic value (and, therefore, likely magnitude of influence), season, site, year and depth were all significant. Although depth remained statistically significant, it was of considerably reduced influence when only subtidal data were analysed. The significance of all the factors included in our model clearly underlines the value of a multi-factorial approach and of having multiple years to include within models.
Table 1

Taxonomic breakdown of recruits encountered on all panels (sites and depths pooled) at Lough Hyne, 1997–2002

Cheilostome bryozoans

  Aetea sp.

Cheilostome ancestrulae

Haplopoma graniferum

Schizoporella unicornis

  Beania mirabilis

Chorizopora brongniartii

Haplopoma sciaphilum

Schizotheca fissa

  Bicelleriella ciliata

Cribrilaria punctata

Hincksina flustroides

Scruparia ambigua

  Bugula flabellata

Cribrilina cryptooecium

Hippothoa sp.

Scruparia chelata

  Bugula sp.

Cribrilina punctata

Lagenoporina sp.

Scrupocellaria reptans

  Caberea boryi

Electra pilosa

Membraniporella nitida

Scrupocellaria scrupea

  Callopora aurita

Escharella immersa

Microporella ciliata

Scrupocellaria scruposa

  Callopora craticula

Escharella labiosa

Omalasecosa ramulosa

Smittoidea amplissima

  Callopora dumerlii

Escharella variolosa

Phaeostachys spinifera

Turbicellepora sp.

  Callopora lineata

Escharella ventricosa

Puellina gattyae

Umbonula ovicellata

  Callopora rylandi

Escharina vulgaris

Schizomavella auriculata

Unidentified cheilostomes

  Cellepora pumicosa

Escharoides coccinea

Schizomavella discoidea

  Celleporella hyalina

Fenestrulina malusii

Schizomavella linearis

  Celleporina hassallii

Figularia figularis

Schizoporella dunkeri

Ctenostome bryozoans

  Alcyonidium sp.

Nolella dilatata

Cyclostome bryozoans

  Crisia denticula

Cyclostome ancestrulae

Diastoporidae sp.

Tubulipora sp.

  Crisia sp.

Disporella hispida

Filicrisia geniculata

Anthozoan cnidarians

  Caryophyllia smithii

Corynactis viridis

Metridium senile

Hydrozoan cnidarians

  Bougainvillea ramosa

Kirchenpaueria sp.

Plumularia setacea

Unidentified hydroid

  Calycella syringa

Lovenella producta

Sertularella sp.

  Halecium sp.

Obelia geniculata

Tubularia indivisa

Calcarea sponges

  Leucosolenia complicata

Sycon ciliatum

Demosponges

  Pseudosuberites sulfureus

Dysidea fragilis

Unidenified demosponge

  Clathrina coriacea

Halichondria panacea

Cirriped crustaceans

  Elminius modestus

Semibalanus balanoides

Verruca stroemia

Ascidian chordates

  Botrylloides leachii

Dendrodoa sp.

Lissoclinum perforatum

Unidentified ascidian

  Botryllus schlosseri

Didemnus sp.

Morchellium argus

Bivalve molluscs

  Anomia ephippium

Hiatella arctica

Monia patelliformis

Mytilus edulis

Other taxa

  Encrusting coralline algae

Foraminifera

Spirorbis sp.

  Erichthonius punctatus

Pomatoceros sp.

Table 2

ANOVA results of temporal and spatial factors influencing variability of recruit numbers on panels at Lough Hyne (2000–2002)

Source of variation

df

Adj MS

F

P

Year

1

45.539

29.57

0.000

Season(Year)

3

169.897

110.32

0.000

Site

1

16.372

10.63

0.001

Depth(Site)

2

84.633

54.96

0.000

Year×Site

1

0.713

0.46

0.497

Year×Depth(Site)

2

5.211

3.38

0.035

Season(Year)×Site

3

0.492

0.32

0.811

Season(Year)×Depth(Site)

6

17.301

11.23

0.000

Error

301

1.540

Total

320

Table 3

ANOVA results of temporal and spatial factors, excluding intertidal data, influencing variability of recruit number on panels at Lough Hyne (1997–2002)

Source of variation

df

Adj MS

F

P

Year

3

26.694

27.78

0.000

Season(Year)

3

370.214

385.32

0.000

Site

1

38.558

40.13

0.000

Depth(Site)

1

16.224

16.89

0.000

Year×Site

3

4.100

4.27

0.005

Year×Depth(Site)

3

2.161

2.25

0.082

Season(Year)×Site

3

1.128

1.17

0.319

Season(Year)×Depth(Site)

3

1.738

1.81

0.145

Error

491

0.961

Total

511

Most variability in recruit numbers was between the intertidal and subtidal (F-values; Tables 2, 3). The most obvious patterns in recruit frequency, in time or space, were fairly regular fluctuations with season (Fig. 2a, b). Variability did, however, remain apparent at other time scales measured—between years and within seasons—and with spatial factors (depth and site). Recruitment in 2001, for example, was high at most site/depths. Besides peak magnitude, there was also variability in other features of the data. The number of recruitment peaks differed; two or three occurred at some sites and depths in some years. The timing and duration of peaks also varied between years and sites. So, although the dominant pattern was a seasonal rise and fall in recruit numbers, other temporal and spatial patterns were clearly superimposed on this (Fig. 2a, b).
Fig. 2

Total recruit levels and the three highest recruiters for each depth at: a Labhra Cliff and b Whirlpool Cliff. Data represented as mean and standard error of three panel replicates

Intertidal data showed differing patterns to those in the subtidal. At the Labhra site, the high intertidal zone recruitment in the year 2000 was the most obvious feature. The level of recruitment masks the pattern of recruitment for 2001 and 2002 if plotted on the same scale. The cause of the 2000 peak was mainly mass recruitment of serpulid polychaetes (Pomatoceros sp.) (Fig. 2a; Table 4). On the intertidal panels at the Whirlpool site there was a lower, more regular, recruitment pattern over the two and one-half study years. Recruitment at this depth/site was dominated by the introduced barnacle Elminius modestus (Table 4; see Fig. 4). Although, like the subtidal data there was a strong seasonal fluctuation, this was manifested by two sets of peaks and troughs per annum—the peaks occurring in the spring and autumn and the troughs in the summer and winter. The depressed summer recruit density contrasted strongly with the raised subtidal levels at the same sites. Notably two features of the data were common to all sites and depths. First the approximate level of baseline recruitment between peaks. Second, the recruitment patterns of just a few taxa were largely responsible for the overall season pattern (taxa illustrated in Fig. 2a, b; Table 4).
Table 4

Major benthos recruitment events at Lough Hyne, with year, depth and site. Data is shown as percentage dominance of specific taxa in terms of recruit numbers. Percentage values shown have been calculated from recruitment over each year

Dominant taxa

Year

Site

Depth

Scale of dominance (%)

Pomatoceros sp.

2000

Labhra

Intertidal

51.38

Elminius modestus

2000

Whirlpool

Intertidal

59.65

Elminius modestus

2001

Whirlpool

Intertidal

97.18

Pomatoceros sp.

1998

Labhra

6 m

71.04

Verruca stroemia

1998

Whirpool

6 m

13.00

Anomia ephippium

1998

Whirlpool

6 m

39.29

Pomatoceros sp.

2001

Labhra

6 m

66.58

Pomatoceros sp.

2001

Whirlpool

6 m

73.61

Pomatoceros sp.

1998

Labhra

12 m

44.81

Verruca stroemia

1998

Labhra

12 m

23.81

Anomia ephippium

1998

Whirlpool

12 m

37.40

Pomatoceros sp.

2000

Labhra

12 m

72.32

Pomatoceros sp.

2001

Labhra

12 m

62.69

Pomatoceros sp.

2001

Whirlpool

12 m

55.10

The taxa recruiting in highest numbers and so dominating the seasonal pattern were Serpulidae (Pomatoceros sp.), Spirorbidae (Spirorbis sp.), Anomia ephippium and Verruca stroemia, in the subtidal of both sites. In the intertidal of both sites the equivalent taxa were Serpulidae (Pomatoceros sp.), A. ephippium and E. modestus. The temporal pattern of none of these taxa, however, mirrored the general trend of recruit numbers.

Variability in recruit-species richness

Season was also a major and striking component of variability in species richness (Fig. 3). Few higher taxa (mainly cheilostome bryozoans) were largely responsible for overall seasonal patterns of species richness. The bimodality and trimodality evident in peak recruit numbers (Fig. 2a, b) was generally smoother, so the seasonal pattern became clearer (except at Whirlpool 6 m in 2001). This may be in part due to peak numbers of species being one to two orders of magnitude below total recruit numbers. Almost necessarily due to the low numbers of species (compared with recruit numbers) seasonal changes were more gradual. The lowest numbers of species were in the intertidal (typically <10). The highest numbers of species occurred at Whirlpool 6 m (~20) in summer (Fig. 3). This contrasted with maximum recruit numbers, which occurred at the Labhra site at 6 m. Overall patterns of bryozoan species richness, due to their domination of species present (Table 1), almost entirely explained the pattern of total species numbers (Fig. 3).
Fig. 3

Mean numbers of recruit species for each site and depth standardised to 30 days submersion (closed circles). Total numbers of most contributory taxa (Bryozoa) are also shown (open circles). Data represented as mean and standard error of three panel replicates

As with recruit numbers, most variability in the number of recruiting species (per 30-day period) occurred between the intertidal and the subtidal. However, there was only, at most, an order of magnitude difference in the number of species recruiting between the intertidal and the subtidal zones. Temporal patterns, other than summer peaks and winter troughs, were apparent. Monthly variability was obvious at the Whirlpool site at 6 m in 2001, and, as such, was different to other years. There was also considerable between-year variation at the Labhra subtidal sites. Site variation was most obvious in the timing and duration of peaks of species numbers.

In contrast to subtidal species richness, the magnitude of intertidal peaks showed major differences between years. There was almost complete dominance by certain taxa (Table 4), but in the year 2000 a large number of taxa recruited in small numbers. Some mobile benthos, such as the sea star Asterias rubens, also had an unusual intertidal pulse of recruitment the same year at Lough Hyne (the only such event between 1997 and 2003, authors’ personal observations).

A four-factor GLM ANOVA on species richness data, including intertidal data, showed depth having the principal influence (Table 5). This influence affected the results to such an extent that we considered its effect might mask the influence of other factors. One significant interaction between terms was evident, which suggested that species richness variability with depth itself varied with season. Within a second GLM ANOVA we carried out an analysis using solely the subtidal data (Table 6), which showed, in contrast, time factors to explain most variability. The greater number of interactions between terms in the subtidal model suggests increased system complexity compared to the intertidal, though season alone explained most variability.
Table 5

ANOVA results of temporal and spatial factors influencing variability of recruit species richness on panels, including intertidal data (2000–2002)

Source of variation

df

Adj MS

F

P

Year

1

20.622

50.40

0.000

Season(Year)

3

24.839

60.71

0.000

Site

1

1.083

2.65

0.105

Depth(Site)

2

79.396

194.04

0.000

Year×Site

1

0.093

0.23

0.635

Year×Depth(Site)

2

0.179

0.44

0.646

Season(Year)×Site

3

0.216

0.53

0.663

Season(Year)×Depth(Site)

6

4.856

11.87

0.000

Error

334

0.409

Total

353

Table 6

ANOVA results of temporal and spatial factors influencing variability of recruit species richness on panels, excluding intertidal data (1997–2002)

Source of variation

df

Adj MS

F

P

Year

3

5.9193

19.08

0.000

Season(Year)

3

47.2280

152.24

0.000

Site

1

0.1238

0.40

0.528

Depth(Site)

1

3.3173

10.69

0.001

Year×Site

3

1.4945

4.82

0.003

Year×Depth(Site)

3

0.5583

1.80

0.146

Season(Year)×Site

3

1.6434

5.30

0.001

Season(Year)×Depth(Site)

3

0.3207

1.03

0.377

Error

495

0.3102

Total

515

Variability in Shannon H′ diversity

Two four-factor GLM ANOVA were carried out at the H′ level and, as with recruit and species number data, most variability was seen between the intertidal and subtidal zones (Table 7). So the depth factor produced the highest F-value in the model, followed by year and season. There was significant interaction between terms, showing that variation in recruitment with depth varies with season. Analysis of just subtidal data (Table 8) showed only temporal factors (year and season) to be significant. A significant interaction between season and site indicated that differences in diversity between sites varied with season.
Table 7

ANOVA results of temporal and spatial factors influencing variability of recruit diversity (Shannon–Wiener H′) on panels, including intertidal data (2000–2002)

Source of variation

df

Adj MS

F

P

Year

1

1.5238

35.20

0.000

Season(Year)

3

1.5692

12.08

0.000

Site

1

0.0298

0.69

0.408

Depth(Site)

2

7.5668

174.81

0.000

Year×Site

1

0.1448

3.35

0.068

Year×Depth(Site)

2

0.0334

0.77

0.464

Season(Year)×Site

3

0.0021

0.05

0.986

Season(Year)×Depth(Site)

6

0.1529

3.53

0.002

Error

334

0.0433

Total

353

Table 8

ANOVA results of temporal and spatial factors influencing variability of recruit diversity (Shannon–Wiener H′) on panels, excluding intertidal data (1997–2002)

Source of variation

df

Adj MS

F

P

Year

3

1.7566

10.30

0.000

Season(Year)

3

0.5846

3.43

0.017

Site

1

0.4023

2.36

0.125

Depth(Site)

1

0.4335

2.54

0.111

Year×Site

3

0.4072

2.39

0.068

Year×Depth(Site)

3

0.1695

0.99

0.395

Season(Year)×Site

3

0.4778

2.80

0.039

Season(Year)×Depth(Site)

3

0.3869

2.27

0.080

Error

479

0.1705

Total

499

The first 2 years of data from the subtidal showed, when analysed by Maughan (2000), significance in only the spatial factors of depth and site (Table 9). Extension and re-analysis of the data set covering 5 years showed temporal effects to be more important than spatial effects. Furthermore, year became a significant term in the analysis of the 5-year data set, whereas it had been insignificant in the 2-year data set.
Table 9

Variability of importance of temporal and spatial factors on diversity (Shannon–Wiener H′) of panel recruits with study length (2 years vs. 5 years)

Source of variation

df

MS

F

P

ANOVA for 1997–1999 from Maughan (2000)

  Year

1

0.0074

0.17

0.678

  Depth(Site)

3

0.2084

4.86

0.002

  Site

2

0.4489

10.47

0.000

  Replicate

2

0.0046

0.11

0.899

  Year×Depth(Site)

3

0.1092

2.55

0.056

  Year×Site

2

0.0029

0.07

0.935

  Error

406

0.0429

  Total

419

ANOVA for 1997–2002 (present study)

  Year

3

1.7566

10.30

0.000

  Season(Year)

3

0.5846

3.43

0.017

  Site

1

0.4023

2.36

0.125

  Depth(Site)

1

0.4335

2.54

0.111

  Year×Site

3

0.4072

2.39

0.068

  Year×Depth(Site)

3

0.1695

0.99

0.395

  Season(Year)×Site

3

0.4778

2.80

0.039

  Season(Year)×Depth(Site)

3

0.3869

2.27

0.080

  Error

479

0.1705

  Total

499

Temporal patterns for specific taxa

Individual taxa showed patterns of recruitment at all temporal scales measured: monthly, seasonal and annual. The magnitude and duration of these recruitment events varied considerably between species, sites and depths. Simple kite plots of example taxa are given in Fig. 4a– f. In the intertidal zone at the Labhra Cliff site (Fig. 4a), E. modestus had approximate spring and autumn peaks, whereas Spirorbis sp. peaks were closer to summer months. A number of taxa in the intertidal zone showed only a major peak in the summer of 2000. Spirorbis sp. recruitment was regularly low and seasonal until late 2002, when a massive peak occurred. A shift in the magnitude of recruitment, such as in Spirorbis sp., can, over short-duration studies, appear as an irregular pattern, though its timing was regular and only the magnitude of the peak was unpredictable. A difference in magnitude of recruitment in the intertidal between sites can be seen by comparison of Fig. 4a versus b. The temporal patterns of subtidal barnacle recruitment (V. stroemia and E. modestus); one recruitment event at about the same time each year differed from that in the intertidal (Fig. 4b). This recruitment event also varied within depths in its magnitude and duration between species and years.
Fig. 4

Selected species recruit numbers represented as “Kite” diagrams from: a Labhra Cliff intertidal, b Whirlpool Cliff intertidal, c Labhra Cliff 6 m, d Whirlpool Cliff 6 m, e Labhra Cliff 12 m and f Whirlpool Cliff 12 m. Data represented as means from three panel replicates

Despite the relatively smooth data on overall recruit and species numbers in the subtidal at both study sites, specific taxa showed a bewildering array of patterns. Irregular patterns were shown by the calcareous sponge Scypha ciliatum at Labhra Cliff, the polychaete Pomatoceros sp., the barnacle V. stroemia, the cyclostome bryozoan Crisia spp. and the cheilostome bryozoan Microporella ciliata. Recruitment of A. ephippium was irregular in magnitude and duration, but initiation was consistent between sites. Some taxa recruited throughout the year, for all years. These included Tubulipora spp., where at Labhra Cliff 6 m (Fig. 4c), over the 5-year study, there were only three sample months where none settled. At Whirlpool Cliff 6 m (Fig. 4d), Tubulipora spp. recruits were recorded in all but one sample month. Similarly, Spirorbis sp. recruits were present except in two sample months, and the cheilostome bryozoan Chorizopora brongniartii was present in all but three sample months.

Discussion

The pattern and process of recruitment by organisms has, for a long time, been known to be extremely complex. Even habitats or species with regular recruitment on one scale can vary considerably on others in space, time or both. Unfortunately our capacity for measuring the scope and scales of these is extremely limited. Whilst some multi-decade studies of recruitment exist for pelagic animals [mostly from fisheries data (Rothschild 2000)], they are rare for the benthos. This 5-year data set, from two sites and several depths, which we present, actually represents one of the longer studies, despite clearly not being long term. The brevity of most recruitment studies clearly restricts the power of analyses to seasonal and sub-seasonal scales, despite strong evidence of often massive inter-annual variability in the few species for which many yearly data sets are available (Cushing 1975; Moran 1986; Dayton 1989). Geographic elements of marine invertebrate recruitment and influences of spatial scale are, however, better understood. For example, the intensity, and diversity, of recruits in different regions (Schoener et al. 1978; Barnes 1996) and on large spatial scales (Caffey 1985; McCook and Chapman 1997; Dulvy et al. 2002) has been compared. There is also considerable literature on differences at the less than 1- 100-m scale (Scheer 1945; Keough 1983; Caffey 1985; Todd and Turner 1986; Roberts et al. 1991; Nandakumar 1995; Archambault and Bourget 1999; Lapointe and Bourget 1999; Smith and Rule 2002). Some studies have even tried to separate different aspects of spatial variability, such as latitude and isolation (Holmes et al. 1997). Using the results of our 5-year study we compared the effects of depth and site, as well as investigating annual variability and sub-annual patterns. Whilst we appreciate that our sample size in terms of years is not high, it is amongst the highest of equivalent studies, and we did find a significant effect of year. Maughan (2000), in contrast, analysed recruitment data from the same locality after just 2 years and found no such year effect. Our findings along both spatial and temporal gradients bear some striking comparisons with the literature.

As a semi-enclosed water body our study site, Lough Hyne, is likely to have a number of hydrographic differences to typical coastal conditions. Greater retention of planktonic larvae within a given locality and opportunities for larvae to locate suitable substratum (Archambault and Bourget 1999) will result from increased bay enclosure. Archambault and Bourget (1999) also found that small bays were more likely to have a greater density of larvae present. They related this to bays with apertures of 1.5–7 km (the aperture at Lough Hyne is only 25 m wide). An extended retention time of water, due to restricted exchange, seems likely to be the crucial aspect (Bassindale et al. 1948, 1957; Kitching and Ebling 1967; Ballard 1996; Archambault and Bourget 1999). The size of the bay also relates positively to the number of species present (larger bays possess more species), in much the same way that larger panels will generally have more species settling onto them (Keough 1984). But certain small areas, such as Lough Hyne, can have highly abundant and diverse communities of sessile invertebrates (Kitching 1987). This may be due to a number of factors such as high habitat heterogeneity, steep environmental gradients (Maughan and Barnes 2000a) or high water retention time of the water, which probably allow for a “build-up” of taxa within the system. It seems intuitively reasonable that such factors may facilitate an abundance of settlement (Fig. 2a, b) compared with adjacent open coastlines (authors’ unpublished data).

Many of the taxa typically recruiting to benthic panels, however, have larvae, which spend very little time in the water column. Although some of the most numerous recruits to the panels at Lough Hyne had planktonic larvae (e.g. spirorbid and serpulid polychaetes), most taxa did not. Hydrographic characteristics of water bodies, therefore, do not seem to explain the abundance and speciose nature of, for example, cheilostome bryozoan settlement (which nearly all have effectively benthic lecithotrophic larvae). Other studies (Turner and Todd 1994; Barnes 1996; Holmes et al. 1997) have also shown colonists without planktonic larvae to be important in early development of subtidal epifaunal communities. An obvious potential answer is that the proximity of adult supply sources is very important, and panel recruits simply reflect the species composition of the immediately surrounding cryptic habitats (Holmes et al. 1997). Osman and Whitlach (1998) showed that this type of local recruitment could control the long-term persistence, and dominance, of particular species, albeit on a larger spatial scale. Indeed at our study site Maughan and Barnes (2000b) demonstrated the presence of a highly speciose and abundant bryozoan community at Lough Hyne. Even at Lough Hyne, however, bryozoans are not the dominant members of the sessile community; other taxa such as sponges and cnidarians occupy considerably more space (Turner and Warman 1991; Bell and Barnes 2002) and almost certainly biomass. Similarly, in environments different from Lough Hyne, such as the Antarctic, bryozoans may dominate recruiting, but not the surrounding species composition (Stanwell-Smith and Barnes 1997). Some of this difference can be explained by differences in r- and K-strategies, timing and duration of larval release, growth speeds and other factors. Much of the time it may largely be a case of good coloniser–bad competitor. So good competitors dominate the more mature surrounding communities, whilst good colonisers dominate panels.

The few medium-term data sets on recruitment to panels do often show a gradual change among recruits (Sutherland and Karlson 1977; Stanwell-Smith and Barnes 1997). Such changes include variation (in space and time) in the importance of individual taxa and colonial versus unitary forms (Schoener et al. 1978). Our data provide a good example of this, showing unitary barnacles to dominate the intertidal panels (as has been widely found across temperate regions) and colonial bryozoans to dominate those in the subtidal. Schoener et al. (1978) linked such species richness to greater habitat variety. Lough Hyne was recognised as early as in the 1920s, to contain a large number of different habitats within a small total area (Renouf 1931). We suggest the high levels of species richness found in the present study can at least be partly attributed to this characteristic.

The striking temporal variation we observed has been observed in a wide variety of environments (Sutherland and Karlson 1977; Dean and Hurd 1980; Mook 1981; Keough 1983; Turner and Todd 1993; Stanwell-Smith and Barnes 1997; Brown and Swearingen 1998) and was noted at Lough Hyne over just 2 years by Maughan (2000). The longer duration of our data, in contrast to most studies, enables some evaluation of annual against sub-annual patterns. Nevertheless, we found the dominant temporal scale, in terms of both recruit numbers and species richness, was season (Tables 2, 3, 5, 6). Just a few species/taxa appeared to give rise to the observed pattern of variation in our data. The massive settlement of Pomatoceros sp. was mainly responsible for the seasonal fluctuation of overall recruits in the subtidal zone, at both sites. Cheilostomatid bryozoans mainly recruited in summer, thereby driving the summer peak of species numbers. However, the main temporal factor explaining diversity (H′) changes was year (Tables 7, 8), whether the intertidal and subtidal were analysed together or not. Thus, we have provided a demonstration that the primary influence on different aspects of recruitment differs with scales and factors measured. This highlights the benefit of long-term, frequently sampled studies, which allow the analysis of data on scales in time and space.

Certain studies have shown that community development is determined by the timing of panel placement (analogous to the opening up of “clean” areas) (Osman 1977; Brown and Swearingen 1998). In contrast, earlier studies (e.g. Scheer 1945) found no essential difference in the community relating to immersion time (timing of events varied but the sequence did not). Although our study was not designed to look at long-term successional patterns, it has identified seasonal patterns of settlement relating to the timing of panel immersion. The varying patterns of temporal settlement observed during this study were in line with the three patterns identified by Keough (1983) for a South Australian assemblage. These include year-round settlement, settlement at regular times of the year and, unlike Todd and Turner (1986), irregular/unpredictable settlement for certain species. Regular settlers tended to vary in the magnitude of recruitment rather than the timing as found by Keough (1983). Species showing apparently unpredictable recruitment in terms of magnitude, timing or duration during the course of our study may, of course, be predictable at larger spatial or temporal scales.

As concluded elsewhere (Todd and Turner 1986), reduced time availability would seem not to explain the differences in recruit numbers found between the intertidal and subtidal. The intertidal panels were only emersed for approximately 2 h per tidal cycle. Surprisingly, and unlike Todd and Turner (1986), no species in this study were found to be exclusive to the intertidal zone, although many species were exclusively found in the subtidal. There may be two explanations for the lack of intertidal specialists: (1) the reduced range of the intertidal zone in Lough Hyne (due to the asymmetrical tidal cycle) and (2) the positioning of panels so low on the shore. Certainly there are encrusting species (e.g. Chthamalus montagui) only found in the intertidal zone at Lough Hyne and elsewhere in SW Ireland (Kitching 1987).

Flow rate has also been shown to be an important factor in determining the composition of communities in a variety of habitats (Ekman 1983; Nowell and Jumars 1984; Maughan and Barnes 2000a, 2000b). Recruitment of marine invertebrates, food availability and survival without dislodgement can be dictated by boundary-layer flow dynamics (Nowell and Jumars 1984). For a field site, Lough Hyne represents a good opportunity to compare flow, as it has amongst the highest and lowest marine flow rates occurring just hundreds of meters apart (Kitching 1987). High flow regimes (such as our study site, Whirlpool Cliff) tend to be dominated by colonial forms (Maughan and Barnes 2000b). High flow environments are often more species rich. Areas of lower flow (Labhra Cliff) tend to be dominated by unitary forms, such as Spirorbis sp. (Maughan and Barnes 2000a).

Differences in early settlers observed at the smallest spatial scale—panel replicates—have been explained by the patchiness of larvae within the plankton or the gregarious nature of many larvae (Keough 1983; Roberts et al. 1991; Wahl 2001). Our protocol, which followed that of previous studies (Todd and Turner 1986; Stanwell-Smith and Barnes 1997; Maughan 2000), attempted to ameliorate issues highlighted by Keough (1983), in which size and proximity of panels to one another were studied. Keough (1983) showed that panels close together (as in the present study) tended to be more similar than those further apart, although recruitment was reduced, due to panels masking one another. Panel size is unlikely to affect the recruitment of species in any active way, as it is improbable that cues have evolved for the selection of a given patch size (Keough 1984). Plankton patchiness has been shown to lead to community differences over small spatial scales (Wahl 2001), which may well lead to differences in the local availability of plankton, particularly for lecithotrophic species. Such pre-recruit patchiness highlights the importance of within- and between-site replication.

In summary, we have demonstrated that, with a multi-year data set examining multiple factors, the interface between the intertidal and the subtidal zones was of overriding importance. Peak monthly levels of recruitment of individuals (~4000 per 10×10 cm panel) and species (~20 per 10×10 cm panel) were decoupled in space but not in time. The relative influence of both temporal and spatial factors and scales dominated different aspects of recruitment and early community establishment. We believe our findings validate our multi-factorial approach, both in terms of investigating differing potential influences and what aspect of the community of individuals might be influenced. Furthermore, in a time of heightened concern about the ecological response to various aspects of global climate change and water quality issues even data sets of a decade’s duration may prove important and rare. Despite many ecologists repeatedly stressing the importance and value of long time series, it is short-term data sets, which are being increasingly presented. If the meagre time span of our study becomes regarded as one of the longer operating with monthly samples—benthic ecology has also become a victim of the shifting baseline syndrome.

Acknowledgements

We would like to thank Dr. J. Bell, I. Davidson, K. Rawlinson and Dr. E. Verling for assistance in fieldwork. We thank University College Cork technicians A. Whittaker and B. McNamara for maintenance of field equipment and D. O’Donnell of Duchas for granting our research permit to work inside the Marine Nature Reserve of Lough Hyne. We also thank Prof. C. Todd (Gatty Marine Laboratory, University of St. Andrews) for making available the experimental apparatus (panels) used in this study. Finally, we would especially like to thank Dr. R. O’Riordan and Prof. T. Cross for comments on the manuscript and Dr. A.-M. Power for assisting with the ANOVA analysis.

Copyright information

© Springer-Verlag 2004