JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

ELSEVIER Journal of Experimental Marine Biology and Ecology,

209 (1997) 103-122

Sedimentation effects on shallow coral communities Kenya

T.R. McClanahan”‘“, D. Oburab

in

“The Wildlife Conservation Society, Coral Reef Conservation Project, P.O. Box 99470, Mombasa, Kenya bRosenstiel School of Marine and Atmospheric Sciences, University of Miami, Florida, USA

Received 31 October 1995; revised 21 April 1996; accepted 31 May 1996

Abstract

Since the early 1960s increased soil erosion due to changing land-use practices in the Sabaki River catchment basin, has increased river-sediment discharge into coastal waters around Malindi, Kenya. Line transect surveys of shallow ( < 5 m at low tide) coral reef communities were conducted in 1985-1988 and 1992-1993 on a gradient of sediment influence in the Watamu (low influence) and Malindi (intermediate and high influence) National Marine Parks. Total algal cover increased between surveys only at the control (low sediment) reef, to levels comparable to the sediment influenced reefs. Within algal categories (turf, calcareous, fleshy and coralline) there were no consistent differences among treatment groups consistent with sediment influence. Soft coral and sponge cover were higher at increasing levels of sediment influence, though this trend is confounded by a parallel increase in water motion. Coral cover increased significantly over time at the intermediate reef, to levels comparable to the low and high-sediment influenced reefs. Generic richness, diversity and dominance of corals were broadly similar among all reefs except for higher dominance in the control reef. Positive correlation between differences in coral genus abundance and differences in mean coral colony sizes over time and among reefs suggests a suite of sediment-tolerant (Echinopora, Galaxea, Hydnophora, Millepora and Platygyra) and sediment- intolerant (Favia, Montipora and Pocillopora) genera. Acropora, Astreopora, Favites and Porites were intermediate between these groups. Reefs exposed to high sediment influence were dominated by sediment tolerant and intermediate coral genera during both surveys, while reefs exposed to low sediment influence were dominated by sediment-intolerant and intermediate genera. Overall, although there were changes in some of the parameters listed above, and in coral genus abundance patterns, no evidence for decreased diversity and ecological health of sediment- influenced reefs could be found for our set of community-level measurements of the shallow-water coral assemblage. Copyright 0 1997 Elsevier Science B.V. All rights reserved.

Keywords: Algae; Coral diversity; Eutrophication; Kenya; Marine protected areas; River dis- charge; Sedimentation

*Corresponding author.

0022~0981/97/$17.00 Copyright 0 1997 Elsevier Science B.V. All rights reserved PII SOO22-098 1(96)02663-9

104 T.R. McClanahan, D. Obura I .I. Exp. Mar. Bid. Ed. 209 (1997) 103-122

1. Introduction

Sedimentation and eutrophication (nutrient addition) are thought to be the major cause of coral reef degradation worldwide (Ginsburg, 1993). The Sabaki River discharges into Kenyan coastal waters of the Indian Ocean near Malindi, and has been cited frequently as an example of marine environmental degradation due to soil erosion upcountry (Bliss-Guest, 1983; Finn, 1983; van Katwijk et al., 1993). Conversion of land from natural forest vegetation to agriculture and grazing over the last 30 years has increased soil erosion (Dunne, 1979) and subsequent transport of sediment to the ocean. The impact of this increased sedimentation and associated nutrient enhancement on regional coral reefs is poorly documented.

Sediment outflow from the Sabaki River is affected by the monsoon-dependent interaction between the two annual river discharge peaks (rainy seasons) and the seasonal reversal of inshore currents (Fig. 1; Brakel, 1984; McClanahan, 1988). Long rains coincide with southeast monsoon winds (SEM, May-November) which entrain inshore currents and river discharge northward over the northern Kenya coast where coral reefs are patchy, small, and generally of low diversity (Samoilys, 1988; McClanahan, 1990). Short rains coincide with northeast monsoon winds (NEM, December-March) which entrain inshore currents and river discharge southward towards high-diversity coral reefs in the Malindi Marine National Park (Hamilton and Brakel, 1984; McClanahan and Mutere, 1994). Consequently, Malindi reef waters are period- ically murky or red colored from upcountry soil starting in December, about 1 month after peak river discharge in November. The duration and magnitude of river discharge over Malindi reefs varies from year to year, due to meteorological variability in monsoon conditions. Heavy rains in November 1961 initiated a period of increased sediment discharge by the Sabaki River. Compounded by increased land use and soil erosion, sediment discharge has probably continued and intensified to the present (Finn, 1982, 1983). Within this trend, the early 1980s and 1991-1992 were drought years in East Africa, punctuated by two years of heavy rain, 1989 and 1992-1993 (Fig. 2). Recent coring of a massive Porites coral in Malindi’s North Reef indicated clearly that increasing amounts of sediment were incorporated into the skeleton in the past 3 decades (Dunbar, Cole and McClanahan, unpubl. data).

Studies of benthic diversity and abundance in Malindi were conducted from 1985 to 1988 and repeated in 1992 and 1993. In the absence of before and after studies, the differential exposure to sediment discharge of these two time periods (late 1980s early 1990s) allows a factorial framework for analyzing sediment effects. Further, the existence of nearby reefs (in Watamu, 1.5 km to the south; Fig. lc) unaffected by river sediment discharge adds a spatial factor for comparisons. Both areas are protected as Marine National Parks, with no extractive uses since 1968. This management allows us to distinguish sediment from extractive use factors. Six predictions concerning the impact of river and sediment discharge on coral-reef substratum cover (summarized in Rogers, 1990) were tested:

Eutrophication and increased sedimentation associated with river discharge is ex- pected to cause:

T.R. McClanahan, D. Obura I J. Exp. Mar. Bid. Ed. 209 (1997) 103-122 105

‘ndi I Watamu rim2 Reserve

DIAN OCEAf

NOV APRIL

- - - Park Boundar

-- Reef Edge

Fig. 1. Sediment plume transport from the Sabaki River mouth during the southeast monsoon (A) and northeast

monsoon (B). The contours indicate qualitative boundaries of suspended sediment concentrations identified by three spectral bands of a LandSat image (solid = high, stippled = intermediate and clear = low) in the Sabaki

River plume in December 1979 (abstracted from Brakel, 1984) and the arrows indicate dominant wind

direction. (C) Map of the Malindi and Watamu Marine National Parks showing study sites: Malindi North Reef Edge, Malindi Coral Gardens, Watamu Coral Gardens and Watamu Lambis Reef.

1.

2.

increased algal abundance as a result of a rapid growth response to nutrient enrichment. increased abundance of soft corals and other heterotrophic benthic invertebrates (filter feeders-sponges, ascidians, etc.) as a result of their rapid growth response to higher enrichment.

106 T.R. McClanahn, D. Ohura I J. Exp. Mar. Biol. Ecol. 209 (1997) 103-122

- 5-year annual - Quarterly moving average

2000

1800

.E 1600.

2 1400

3 1200

d 1000

-~

8 800

k 600 AZ 8 400

B 200

0

1952 1956 1960 1964 1968 1972 1976 1980 1984 1988 1992

Year

2500,

1 2000

s

g 1500 1

B z 1000

e

I-' 500

- Monthly average

Jan 90 Jan 91 Jan 92 Jan 93 Jan 94

Fig. 2. (a) Sabaki River quarterly and 5.year moving average river discharge, 1953-first quarter 1992, in

millions of cubic meters. Data from the Ministry of Water Development, Kenya Government (1993). (b)

Sabaki River turbidity, monthly averages from May 1989 to April 1994, in Nephelometer Turbidity Units.

Data from Kenya Pipeline and Water Conservation Corporation.

decreased hard coral cover due to metabolic costs of shedding sediments and interference and resource competition with algae, soft corals and other benthic

species (see predictions 1) and 2) above). decreased coral species and genus richness due to mortality of species vulnerable to competition and sediment-related stress. decreased diversity and increased dominance of corals due to selective survivorship of resistant species. change in coral colony size: two contrary predictions are that a) average coral colony size will be smaller due to partial mortality, slower growth associated with

sedimentation, and greater sediment-shedding efficiency for small colonies, or b) colony size may increase due to selective survival and growth of species more resistant to stress, and reduced recruitment success.

T.R. McClanahan, D. Obura I J. Exp. Mar. Biol. Ecol. 209 (1997) 103-122 107

2. Methods

2.1. Study sites

Sites are hard substratum, patch reef coral communities common along the East African coast (Hamilton and Brakel, 1984; McClanahan and Mutere, 1994), and protected from fishing for over 20 years. The Malindi reefs are a series of nearshore platform reefs with exposed and sheltered faces that rise above a sand plain that is seldom deeper than 7 m at low tide. The northern tip of the North Reef (Fig. lc) faces directly north towards the Sabaki River mouth and is exposed to waves and swell from the ocean. Two locations were surveyed-a shallow patch reef ( < 2 m deep at mean low water, MLW) and a deeper reef edge community ( < 5 m deep at MLW). The second study area on the Malindi reef was a sheltered lagoon coral community (Fig. lc, < 1.5m deep at MLW), surrounded by an emergent reef platform except for a narrow channel to the west. The Watamu reef is fringing, and study sites were selected in the lagoon ( < 2 m deep at MLW, Fig. lc). A sheltered location has been the main study site since the 1980s with the addition of a more wave-exposed site 500 m to the south, in 1992. Data from the two control reefs were combined for the 1990s.

These reefs represent three treatment levels of exposure to sediments:

Control (low)-the Watamu sites experience low river sediment exposure and a range of wave exposure from low to high. Intermediate-the Malindi Coral Gardens are sheltered from heavy waves and currents and are exposed to sediments that have traversed outer reef edges. High-the northern tip of the Malindi North Reef is exposed to strong waves and currents, and to sediments directly from the Sabaki River. Resuspension of in-situ sediments by rough water can occur year round, converting acute river discharge effects to chronic sediment resuspension.

2.2. Data sources and field methods

Overall 17 reef censuses totalling 284 10-m line transects were sampled in two time periods: 1985-1988 and 1992-1993. The censuses were conducted as sections of four different research efforts. The early censuses on the Malindi North Reef edge (1985 and 1987) used a smaller subset of cover types than the standard categories adopted for later censuses. The Watamu and Malindi Coral Gardens censuses in 1987 did not identify coral to the genera. For statistical analysis the censuses were grouped into six ‘treatments’ defined by time (1980s versus 1990s) and sediment exposure (control, intermediate and high), though some comparisons could not be made due to missing data from the earlier censuses.

Placement of the 10-m transect lines varied with the different research efforts, however all were placed within a homogeneous community, the coral dominated, hard substrate patch reef zone. The transects were draped loosely on the bottom and used to measure the canopy organism’s length under the line (crown length for corals) with a flexible tape measure (in cm) or by counting chain links (of 1.2 cm length). Relative

108 T.R. McClanahan, D. Obura I .I. Exp. Mar. Bid. Ed. 209 (1997) 103-122

abundance of each cover category was expressed as the percentage of total transect length. Cover categories censused were coral genera, soft coral, sponge, algae (turf, fleshy, calcareous (Halimeda) and crustose coralline), seagrass and sand (McClanahan and Shafir, 1990). Percent values were arcsine transformed for ANOVAs (Sokal and Rohlf, 1981) though raw percentages are presented for ease of interpretation in figures and tables. Calculations included an index of dominance (dominant coral genus/total coral cover) and diversity (Simpson’s Index, D = 1 - C pf).

Water transparency (visibility) and sedimentation were measured during 1992 and 1993 at the high sediment site in Malindi and the control site in Watamu. Visibility was measured horizontally using a Secchi disk 0.5 m off the bottom at low tide between 8 AM and 4 PM. Sedimentation rates were measured by the mass of filtered and dried sediment accumulated on 15*15 cm ceramic tiles, exposed for variable periods from 7 to 30 days. For comparison of this method with the more standard tubular traps, tubular sediment traps were also deployed ( > 3: 1 height to diameter ratio, = 7.5 cm diameter: Gardner, 1980; Buessler, 1991). Water flow was measured with a mechanical flow meter (General Oceanics Digital Flowmeter) over 0.5-2.0 h intervals at low tide, 0.5 m off the bottom at the 4 study sites.

3. Results

3.1. Water quality

River discharge data were available for the Sabaki River from 1953 until 1992 (Fig. 2a). Some months in the series were missing, so values were interpolated scaled on monthly weights and annual totals. The 1961 discharge peak during the last quarter (northeast monsoon, NEM) is clearly visible. The other high discharge peaks fall in the second quarter, corresponding to the southeast monsoon (SEM) and thus do not affect Malindi reefs. Discharge is low through most of the 1980s with a sharp increase in 1989. Discharge in 1990-1992 is lower (and more consistent) than in the 1980s. A turbidity data set was only available for 1989-1994 (Fig. 2b), but clearly shows the two seasonal rainfall peaks in the northeast (November-December) and southeast (April-June) monsoons. The unusually high rainfall in the northeast monsoon of 1992-93 stands out as a higher and broader peak, with failed southeast monsoon rains five months later.

Water visibility in Watamu was highest during the NEM and lowest in the SEM (Table 1). The reverse occurred in Malindi, with lowest visibility during the NEM coincident with river discharge and highest visibility during the SEM, in the absence of river discharge. Variation in visibility was highly significant between reefs (F = 254, p < 0.001; Table 1). Variation in visibility as the main ANOVA factor ‘monsoon’ was not significant due to the opposite trends in the two reefs mentioned above, resulting in a highly significant interaction term (reef*monsoon, F = 21, p < 0.001; Table 1).

Sedimentation rates were measured at sheltered and wave-exposed sites in both Malindi and Watamu (though the sheltered Malindi site is not the Coral Gardens used in these censuses). ANOVA of log-transformed sedimentation rates (Table 2) indicates that

T.R. McClanahan, D. Obura 1 J. Exp. Mar. Biol. Ecol. 209 (1997) 103-122 109

Table 1 Analysis of variance of visibiiity (in meters, horizontal Secchi disc readings) among reefs (Malindi vs.

Watamu) and season (northeast monsoon, NEM vs. southeast monsoon, SEM)

Visibility (meters)-Analysis of Variance

Descriptive statistics

Malindi Watamu

NEM SEM NEM SEM

Mean 7.034

S.D. 4.24

n 92

Analysis of Variance: r2 = 0.495

ss

9.43 16.55 14.66 3.25 3.38 4.99

74 76 63

d.f. MS F P

Reef 4067.6 1 4067.6 254.4 <O.OOl ***

Monsoon 4.7 1 4.7 0.3 0.59 ns

Reef*Monsoon 344.5 1 344.6 21.6 <O.OOl *** Error 4811.9 301 16.0

the two Malindi sites were not significantly different, similarly for the two Watamu sites, but that Watamu and Malindi sites were significantly different, with p < 0.001. Linear regression of sedimentation rates measured by tubular traps on those measured by tiles explained just under 50% of the variation between methods, and indicates a factor of 3 is necessary to scale tile-rates up to trap-rates (Table 2).

Water flow was measured during the 1993 SEM and 1993-94 NEM. ANOVA and a posteriori comparisons indicate that mean water flow during the SEM is similar among all reefs, but lower in the sheltered reefs during the NEM (Chi-squared, p -=c 0.023). Wave heights were not measured, though during heavy swell and storms waves up to 1.5-2.5 meters high can pass over the ‘exposed’ sites at low tide. At the sheltered sites, wave heights at > 0.5 m at low tide were never observed.

3.2. Algal cover

Algal cover is presented as a total and broken down into four categories (Fig. 3a, Fig. 3b, Fig. 3c, Fig. 3d, Fig. 3e). Following arcsine transformation of relative cover, there was still significant heterogeneity of variance for all five groups (Bartlett’s test, p < 0.001 for all), thus ANOVA was not performed. Total algal cover in Watamu increased from the 1980s to the 1990s but remained the same at both Malindi reefs (Fig. 3a). Total algal cover at the high siltation site was consistently less than at the intermediate site for both time periods. Algal turf cover showed less consistent variation among reefs and times (Fig. 4b)-in the 1980s algal turf was more abundant at the high siltation site than both intermediate and control sites. In the 1990s there were no significant differences in algal turf cover among the sites, due to an increase in abundance at the control site, and decreases at both intermediate and high siltation sites.

110 T.R. McClamhun, D. Oburrr I J. Exp. Mar. Biol. Ecol. 209 (1997) 103-122

Calcareous (i.e. Halimeda) and fleshy algal cover (Fig. 3c and Fig. 3d) followed a similar pattern, decreasing in abundance at higher siltation sites in Malindi. Both increased in abundance from the 1980s to 1990s at the control reef, and calcareous algae increased in abundance from the 1980s to 1990s at the high siltation site. No data were available for fleshy algal cover at the high-siltation site in the 1980s. Coralline algal cover (Fig. 3e) was higher at the intermediate siltation site at both times, and increased in abundance from the 1980s to 1990s with the exception of the high-siltation site in the 1980s. for which no data were available.

Table 2

a) Sedimentation rate (mg/m2/day) in Malindi and Watamu, at rough and calm sites. Descriptive statistics and

Analysis of variance among reefs. b) Linear regression of ceramic tile on tubular trap methods for measuring

sedimentation

Sedimentation rate, mg/cm*/day

Descriptive statistics

Malindi Watamu

Calm Rough Calm Rough

Mean 4.25

S.D. 5.57

n 96

Bartlett test, homogeneity of variance

3.11 1.35 0.89

4.38 1.62 1.06

87 60 40

Chi- d.f. P

square

log-transformed data 2.76 3 0.43

Analysis of variance (log transformed data)

r2 = 0.22

ss d.f. MS F P

Between 106.88 3 35.63 25.36 <O.OOl

Within 390.47 278 1.41

A posteriori multiple comparisons, Tukey HSD

Mal-calm Mal-rough Wat-calm Wat-rough

Mal-calm

Mal-rough ns Wat-calm *** ***

Wat-rough *** *** ns

Linear Regression: trap = slope *tile + constant

Dependent variable: trap n = 20 r* = 0.462

Variable Coefficient Std. Error ‘t’ p (2-tail)

Constant 1.92 3.88 0.49 0.63

Slope 3.21 0.82 3.93 0.001

T.R. McClanahan, D. Obura I J. Exp. Mar. Bid. Ecol. 209 (1997) 103-122 111

a) Total algae 80 , I

b) Algae - turf c) Algae - calcareous C”

5o .............

60 1 ....................................................

~~.~.~..................~................. 4. _ @I 15

............................................... .... ._ ... 40 30 10

20 20

10 5

0 0 0

ctrl lnterm High ctri Interm Wigh ctrl I nterm High

e) Algae - coralline

,O1

f) Soft Coral

257

d) Algae - fleshy 10,

ctll lnterm High ctri Interm High

h) Coral

5o1

ctrl Interm High ctrl I nterm High

ctrl Interm ltigb

i) Coral genus richness

lo1

ctrl lntera High

63 1990’5

n 1990’S

Fig. 3. Abundance of benthic cover categories and coral genus richness (xksem) in the six reef*time

categories-control, intermediate and high sediment influence versus 1980s and 1990s. (a) total algae, (b) algal

turf, (c) calcareous algae, (d) fleshy algae, (e) coralline algae, (f) soft coral, (g) sponge, (h) coral, and (i) coral

genus richness. Striped columns = 198Os, solid columns = 1990s. Notes:-algal turf: intermediate reef 199Os-

standard error is too small to show at present scale (s.e.m. = 0.004); sponge cover, 1980s~though sponge cover

was a category in use, none were recorded though this may be due to sampling strategy than absence of

sponges. The zero values are ignored in analysis. nd-no data collected (1980s) due to smaller subset of cover

categories.

3.3. Heterotrophic invertebrates

Following arcsine transformation of relative cover, there was still significant hetero- geneity of variance for both soft coral and sponge cover (Bartlett’s test, p < O.OOl), thus ANOVA was not performed. Soft coral cover was highest on the high-siltation reef, both in the 1980s and 1990s (Fig. 3f). It increased over time in the control and intermediate- siltation reefs but remained stable at the high-siltation reef. Sponge cover was low at

112 T.R. McClanahan, D. Obura I .I. Exp. Mar. Biol. Ed. 209 (1997) 103-122

Number of transects

Fig. 4. Cumulative coral genera as a function of the number of 10-m transects for each reef*time category. The total number of transects per category is indicated in the key.

both control and intermediate-siltation reefs, and higher at the high-siltation reef (Fig.

3g).

3.4. Coral cover

Arcsine transformation of coral cover resulted in homogeneity of variance among groups, an ANOVA showing that both reef (3 groups) and time (2 groups) varied significantly (p < 0.05), with a significant interaction term (p < 0.01). Coral cover was stable at about 30 to 35% at the control and high-siltation reefs in the 1980s and 1990s (Fig. 3h). At the intermediate-siltation reef there was a significant increase in coral cover from 20% in the 1980s to 34% in the 1990s.

3.5. Coral richness

Coral genus richness was expressed in number of genera per 10-m transect. Higher richness was sampled at all reefs from the 1980s to 1990s with greatest increases at the control and intermediate reef (Fig. 3i). Fig. 4 shows the cumulative number of genera found with additional transects sampled. The cumulative richness profiles at the control site in the 1980s and 1990s were similar at 16 transects but the 1990s data reached 25 genera in 22 transects. At the intermediate site cumulative genera richness peaked at similar values in both 1980s and 1990s (22 and 23 genera respectively), but the smaller number of transects in the earlier census resulted in a steeper profile for the 1980s (15 versus 35 transects). At the high-siltation reef the cumulative genera richness curves and sampling effort were similar for both the 1980s and 1990s.

3.6. Coral diversity and dominance

Simpson’s Diversity Index (D) were high ( > 0.80) at all sites and varied by less than

T.R. McClanahan, D. Obura I J. Exp. Mar. Bid. Ecol. 209 (1997) 103-122 113

Table 3

Diversity, dominance and Porites relative abundance in study reefs. Diversity is Simpson’s ‘D’ statistic, and

dominance is the relative abundance of the most abundant coral genus

Diversity, D Dominance Porites

1980s Control 0.89 0.20 20

Shelter 0.95 0.30 5

Exposed 0.86 0.24 21

1990s Control 0.80 0.29 18

Shelter 0.83 0.31 14

Exposed 0.86 0.22 21

15% for all time and treatments. Diversity was lowest at the control reef in the 1990s and highest at the intermediate-siltation reef in the 1980s (Table 3). Diversity decreased in the control and intermediate-siltation reefs over time, but remained the same in the high-siltation reef. The dominance index (proportion of the most abundant genus) was highest in the intermediate-siltation site in the 1980s and 1990s. Dominance increased in the control and intermediate-siltation reefs over time, while decreasing in the high- siltation reef. The proportional abundance of Porites was stable at the control and high-siltation reefs (at 20%) and increased from the 1980s to 1990s at the intermediate- siltation reef.

The relative cover of the 12 most abundant coral genera (Fig. 5) is ordered by aggregate abundance (grand average over all reefs*times). At the control reef (Fig. 5a), Montipora, Pocillopora, Astreopora and Favites are more abundant than the grand average in one or both of the censuses. By contrast, Galaxea, Echinopora, Hydnophora,

Milleporu and Plutygyru are less abundant. At the intermediate-siltation reef (Fig. 5b), Acropora, Galaxea and Echinopora are more abundant than the grand average. Porites, Montipora, Hydnophora and Platygyra increase in relative abundance between censuses from below-average levels in the 1980s. Astreoporu and Fuvia were not recorded at the intermediate-siltation site. At the high-siltation site (Fig. 5c), Porites, Galaxea, Hy-

dnophora, Millepora and Platygyra are at high abundance in one or both censuses while Montipora, Pocillopora, and Astreopora are at below-average abundance.

Rank order differences in the relative abundance of genera are shown in Table 4 (see caption for details). Positive numbers indicate higher abundance in high-sediment conditions, negative numbers indicate higher abundance in low-sediment conditions. Porites, Galaxea, Echinopora, Hydnophora, Millepora and Platygyra show higher abundance under the influence of sediments, while Montipora, Pocillopora, Favia,

Favites and Astreopora are at higher abundance under control conditions. Acropora shows intermediate behavior, though there is one more negative than positive difference (4 vs. 3 respectively), the positive differences are larger in magnitude.

3.7. Coral colony size

Differences in mean coral colony crown length were analyzed for the 12 most abundant genera (see Fig. 5). As with genus abundance, a summation over all comparisons was computed to show whether colony size increased or decreased on a

114 T.R. McClanahan, D. Ohura I J. Exp. Mar. Bid. Ed. 209 (1997) 103-122

a) Control

Ml

301L?j b) Intermediate

30

1

c) high-sediment

* Overall q 80’s 90’s

Fig. 5. Coral genus abundance in (A) control, (B) intermediate, and (C) high sedimentation reefs. The line

indicates aggregate genus abundance proportions over all reef*time categories, with genera ordered on the

x-axis. The columns indicate each reef*time category, illustrating deviation from the overall average.

gradient of sediment exposure (Table 4). Galaxea, Echinopora, Acropora, Hydnophora, Millepora, Platygyra, Favites and Astreopora showed an increase in colony size under high-sediment conditions. Pocilloporu, Favia and Montipora showed decreases in colony size under high-sediment conditions. Porites showed intermediate behavior, with one more decrease than increase in size, but a higher magnitude of size increases.

Differences in colony size were contrasted with differences in relative abundance using Kendall’s tau (a non-parametric correlation coefficient; Sokal and Rohlf, 1981). The significant positive correlations (p < 0.01, Table 4), indicates that coral species at

T.R. McClanahan, D. Obura I J. Exp. Mar. Biol. Ecol. 209 (1997) 103-122 115

Table 4 Net positive and negative differences among reef*time groups for cover (percent) and mean colony size of the

12 dominant genera (see Fig. 5)

Differences: abundance versus size

Genus Relative

abundance

(%)

Colony size

(cm)

Rank

correlation

Galaxea 73.23 71

Hydnophora 28.59 162

Millepora 20.55 48

Echinopora 18.68 68 Porites 15.86 24

Acropora 12.09 25

Platygyra 7.21 -8

Favia -1.43 -10

Favites -5.96 52

Astreopora -23.87 9

Pocillopora -59.94 -120

Montipora -75.5 -74

Kendall’s Tau

0.67

P co.01

Differences calculated by subtracting lower levels of sediment influence and earlier times from higher levels

and later times for valid comparisons (i.e. Intermediate 1990s-Intermediate 1980s; High 1990s-Intermediate

1990s; see Table 4). Net positive indicates larger values associated with larger amounts and longer time of

sediment influence. Net differences and magnitude of differences are shown. Correlation (Kendall’s tau)

between cover and colony size for net and magnitude of differences is given. Critical values for n = 12 are

0.455 for alphati0.05 and 0.576 for alphae0.576. The ranking summarizes comparisons of high vs. low sediment influence-i.e. between reefs (high-inter-

mediate-control) and over time (199Os-1980s).

higher relative abundance in high-sediment conditions have larger colony sizes, and vice versa.

4. Discussion

The inability to predict a priori the effects of sediment influence at a given site is a notorious problem (Rogers, 1990). Examples of no or low impact of large amounts of sediment are as numerous as examples of detrimental effects (for example, Glynn and Stewart, 1973; Fisk and Harriott, 1989 for low impact, Loya, 1976; Cortes and Risk, 1985; Acevedo et al., 1989 for high impact, and Rogers, 1990 for a review). Rapid recovery from intense sediment damage has also been reported (Brown et al., 1990). Many studies have been undertaken in areas where compounding anthropogenic influences may introduce interactive effects such as fishing (Tomascik and Sander, 1985) nutrient enrichment (Dodge and Vaisnys, 1977; Chansang et al., 1981; Hunte and Wittenberg, 1992), and hurricanes and other physical disturbances (Fisk and Harriott, 1989).

The coral-reef system studied in this paper is an unplanned experiment on the

116 T.R. McClanahan, D. Obura I J. Exp. Mar. Bid. Ed. 209 (1997) 103-122

influence of sediments in the absence of some of these external factors. All the reefs studied have been protected from extractive uses (fishing, coral and she11 collecting) since 1968, and are demonstrably more diverse than unprotected reefs (McClanahan, 1994; McClanahan and Mutere, 1994). Herbivorous fish such as parrot and surgeonfish are abundant at all studied sites (- 500 kg/ha; McClanahan, 1990) and have remained stable and near their theoretical upper limits (McClanahan, 1992; McClanahan and Obura, 1995). Kenyan reefs do not experience hurricanes (latitude = 3” S) but rather predictable and less intense monsoon storms during the south-east monsoon (McClanahan, 1988). Consequently, we believe our experimental design is robust for testing the effects of moderate and pulsed sediment in the absence of other interactive human and natural impacts.

A previous study of Sabaki sediment influences on Malindi-Watamu reef communities which looked at the association between cover of soft corals, ‘coral injury’ and the abundance of terrigenous sediments in the water and benthic substrates (van Katwijk et al., 1993) found poor relationships with any of these single variables but a stronger relationship when combining the three variables by a canonical correlation analysis which weights variables to find the highest possible correlation. The combination of variables was considered to be a response to sediments stress although the causes of coral injury, relative soft coral and bare rocky substrate cover were not determined experimentally. In contrast to our study this study reported moderate levels of terrigenous sediments in some Watamu areas while our study showed much lower sedimentation levels in Watamu compared to Malindi. Our data, observations and landsat imagery (Brakel, 1984) do not support the contention that significant amounts of river sediments travel as far as Watamu and the source of terrigenous sediments in their samples remains obscure. Further work is required to reconcile the differences between these two studies and more in situ experimental work is needed to distinguish cause and effect relationships between sediments and coral injury.

4.1. Water quality

Variation in environmental conditions and a lack of long-term environmental monitoring data preclude simple and definitive statements explaining sediment influence at different reefs and times. Missing data in long-term river discharge records unfortunately coincides with critical periods in our analysis (1989 and 1992-93) necessitating juggling river discharge and turbidity data (Fig. la, Fig. 1 b), to obtain an overall temporal picture.

A - 2 m length core removed from a massive Porites head in Malindi’s north reef edge (Fig. lc, the most sediment exposed study site) clearly shows, by incorporation of sediment and coloration in the core, the history of sedimentation on this reef (Dunbar, Cole and McClanahan unpubl. obs. and data). The bottom - 1.7 m of the core is white, at - 0.3 m from the top of the core periodic bands of brown coloration are visible and the top 0.1 m the core is continuously brown. These observations support the contention that river sediments and their incorporation into Porites skeleton have increased in the last 3 decades from low to chronic levels.

Spatially, comparison of visibility (Table 1) and sedimentation rates (Table 2) in

T.R. McClanahan, D. Obura I 1. Exp. Mar. Bid. Ed. 209 (1997) 103-122 117

Malindi and Watamu confirm the greater influence of sediments in Malindi not only during the NEM, but extending throughout the year. Further, the influence of river discharge in Malindi is large enough to cause a reversal of the normal periodicity of water clarity (high in the late SEM to early NEM and low in the late NEM and early SEM) as found in Watamu (Table 1; Obura, 1995) and off Tanzania (Newell, 1959; Bryceson, 1982; McClanahan, 1988).

Sedimentation rates measured in Malindi (3 to 4 mg/cm*/day) were low compared to most other studies, from which a threshold rate of 10 mg/cm*/day is estimated to separate ‘normal’ from ‘high’-sediment conditions (Rogers, 1990). By contrast, visibility was clearly low ( < 9 m) for a coral-reef environment. Both sedimentation rate and visibility depend on water turbulence. High tidal fluxes in East Africa (Kenya Ports Authority, 1994) combined with seasonal variation in water conditions (Table 3) contribute to high turbulence and consequently the low sedimentatiomhigh visibility conditions in Malindi.

4.2. Algal cover

Algal cover was not higher under the influence of sediments either spatially or temporally, in fact the sediment-influenced reefs had lower overall algal abundance than the control reef. No consistent patterns were distinguishable among algal categories. One confounding factor that was not addressed in this study is the proximity of the Watamu sites to a large mangrove creek that discharges ‘green’ (nutrient rich) water into the Watamu lagoon on a tidal cycle. The magnitude of this nutrient subsidy relative to the sediment-related effect in Malindi is unknown. Additionally, the top-down control of herbivorous fish on algal biomass (Littler et al., 1983; Hay et al., 1983; Carpenter, 1986; McClanahan et al., 1994) may prevent the algal build-up expected in Malindi as a result of sediment-nutrient enrichment. Observations suggest that only a thin turf grows on substrates after sediment pulses but this disappears after water clarity improves.

4.3. Heterotrophic invertebrates

Heterotrophic invertebrates were more abundant on reefs more exposed to sediments, but changes over time were small. Water motion also enhances heterotrophic invertebrate abundance, and since water motion was highest at the high-siltation site in Malindi, strengthens any potential effect of sediment exposure and makes it difficult to separate the role of water motion versus sedimentation/eutrophication on their patterns of distribution and abundance. Broader surveys on deeper reefs in Watamu (with no sediment and low\intermediate water motion; Obura, 1995) recorded high abundance of soft corals from the family Xeniidae. In contrast the dominant soft corals on the reefs sampled in this study were alcyoniids (though this distinction was not recorded during the surveys). That study postulated that the larger-polyped, fleshy alcyoniids are more resistant to sediment (and water motion) than the small-polyped, creeping xeniids, thus sediment effects may be expressed more by substitution of soft coral species rather than by changes in overall soft coral abundance.

118 T.R. McClanahan, D. Obura I .I. Exp. Mar. Bid. Ed. 209 (1997) 103-122

4.4. Coral cover and diversity

Coral cover and diversity were basically stable over the course of this study, with the

exception of increased coral cover, more equitable cumulative genus richness, decreased Simpson’s diversity and increased cover of Porites at the intermediate reef from the 1980s to the 1990s. The chance inclusion of a large mono-specific Montiporu colony in the 1990s sample at the control reef caused a decrease in diversity and increase in dominance, but with no significant changes in other coral genera. Shallow East African reefs are characteristically dominated by Acroporu, Porites and Galaxea (Hamilton and Brakel, 1984; McClanahan and Mutere, 1994), and are consistent with reef zonation patterns for the Western Indian Ocean (Rosen, 1971; Braithwaite et al., 1973). The similarity in the asymptotes of the cumulative genus curves (Fig. 4) for all reef*time groups suggests a common coral fauna1 group for these reefs, enabling straight-forward comparisons between genera.

The expected reduction in coral genus diversity and increase in dominance with increased sediment influence was not found. The diversity/dominance relations and genus abundance suggest two contrasting patterns: (a) that the genera Porites, Galaxea, Echinopora, Hydnophoru, Millepora and Platygyra are more resistant to sediment/ eutrophication as indicated by their higher abundance in the Malindi reefs. By contrast, Pocillopora and Favia are more abundant on the control than on the sediment reefs and may therefore be less tolerant of sediment effects; and (b) that the coral communities at the exposed and control reefs have remained relatively stable between the census periods while the intermediate reef was undergoing changes in relative genus abundance and total coral cover. These differences suggest present stability in the high-sediment reef may reflect past changes that stabilized before the 1980s census, while differences between censuses at the intermediate reef may reflect a slower or incomplete response to less extreme sediment conditions.

4.5. Coral colony sizes

There was no single trend in mean colony size to select among the opposing hypotheses presented. Instead, some coral genera had larger mean colony sizes associated with high sediment conditions, while some had smaller mean colony sizes. While this may be expected due to sampling error, the significant positive correlation of mean colony size with abundance (Table 4) suggests there is some sediment-related effect. Genera that were more abundant under high-sediment conditions had larger mean colony sizes under these conditions, while genera more abundant on control reefs had smaller mean colony sizes when exposed to sediment. This suggests that corals more common in high-sediment conditions (i.e. sediment resistant) increase in size with sediment influence, while those less common in high-sediment conditions (i.e. non- resistant) decrease in size-whether sediment influence causes an increase or decrease in colony size may be dependent on a species’ life history characteristics such that hypothesis 6a. or b. may be true in different species.

Coral colony size may also be affected by population parameters. Recruitment and

T.R. McClanahan, D. Obura I J. Exp. Mar. Bid. Ed. 209 (1997) 103-122 119

dispersal limitation have been suggested (Sale, 1980; Doherty and Fowler, 1994a,b) to have a greater impact on adult marine populations than factors affecting the adults themselves (although see Shulman and Ogden, 1987). The Malindi reefs are set in a system of offshore platform and fringing reefs while the Watamu reefs are part of a linear fringing reef. Coral spat < 25 mm in diameter are twice as abundant in Malindi than Watamu (Obura, 1995), suggesting recruitment may be enhanced by the greater spatial heterogeneity of the Malindi reef system (on the order of loos-1000s of meters), and that sedimentation levels are not at a level that inhibits coral recruitment (Babcock and Davies, 1991; Hunte and Wittenberg, 1992). It is not known if this difference in recruitment is large enough to have an effect on adult populations, but it is possible that higher recruitment to Malindi reefs may help prevent the decline in coral communities that were initially predicted.

Recruitment and growth rates also affect the size-class distributions of corals. Coral colony size has been hypothesized to relate to sedimentation in two opposing ways (Rogers, 1990): (a) smaller corals are more efficient in removing sediments from their surface, and (b) larger mean colony size may reflect reduced larval recruitment and decreased numbers in smaller size classes. Also, small size may represent reduced growth rates and slower transitions into larger size classes. In this study sediment- tolerant genera had a larger mean colony size in high-sediment conditions while sediment-intolerant genera had a smaller mean colony size.

In conclusion, this study compares coral reefs over a time of continuing and potentially increasing sediment/eutrophication stress and a spatial gradient of sediment influence. Our results do not support many of the ecological predictions that we made. The overall conclusions are not as simple as predictions would suggest:

1. Reduced coral cover and diversity were not in evidence at either the intermediate or the high levels of sediment influence. Patterns in coral diversity, coral cover and algal cover indicate that the Malindi reefs were comparable to healthy reefs outside the influence of the Sabaki River.

2. The coral community on the high sedimentation site has been relatively similar over a period of time (1985 to 1993), suggesting stabilization of the coral community with a greater abundance of sediment-tolerant coral genera and soft corals, relative to control reefs.

3. Lower levels of sediment influence at the intermediate site have exerted less pressure, with the result that the coral community is between a typical control reef and the high-sediment reef. This reef appears to have changed more than the heavily sedimented reef which may have already stabilized.

In the face of worldwide degradation of coral reefs close to human settlement (Ginsburg, 1993) it is encouraging to note that the corals in the shallow reefs in the Malindi Marine Park are not excessively stressed by sediments from the Sabaki River. Interactions between sediment stress and other factors (e.g. herbivory, recruitment) may be critical and thus the protective management of Malindi and Watamu reefs must be regarded as a crucial factor that has helped maintain ‘normal’ reef function in the region.

120 T.R. McClanahun, D. Obura I J. Exp. Mar. Biol. Ecol. 209 (1997) 103-122

Protection of coral reefs from multiple and interactive human influences appears to increase the resiliency of reefs to single influences.

Acknowledgments

Research was completed while the authors were supported by a number of research grants. These include grants to the first author by the East African Wildlife Society, The Pew Charitable Trust, Conservation, Food and Health Foundation, and Grant No. HRN-5600-G-2050-00, Program in Science and Technology Cooperation, Office of the Science Advisor, U.S. Agency for International Development. Funding for the second author was provided by The Rockefeller Foundation. Research permission was granted by the Office of the President, Kenya, data was provided by the Ministry of Water Development and Kenya Pipeline and Water Conservation Corporation, and logistic assistance in the Parks was provided by Kenya Wildlife Service. The field assistance of N.A. Muthiga, J.C. Mutere and S.H. Shafir is greatly appreciated. We thank P. Glynn, S.R. Smith and two anonymous reviewers for their comments on earlier drafts.

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