seagrass estuary in northern New Zealand

Estuarine, Coastal and Shelf Science 66 (2006) 97e110 www.elsevier.com/locate/ecss

Benthic macro-invertebrate community composition within a mangrove/seagrass estuary in northern New Zealand Andrea C. Alfaro Division of Applied Sciences, Faculty of Health and Environmental Sciences, Auckland University of Technology, Private Bag 92006, Auckland 1020, New Zealand Received 6 December 2004; accepted 25 July 2005 Available online 26 September 2005

Abstract In the tropics and sub-tropics, estuarine environments with mangrove and seagrass habitats provide important structures and resources for diverse communities of benthic organisms. However, temperate estuarine habitats, especially in mangrove areas, may differ significantly in their community associations and interactions. The community composition of benthic macro-fauna was investigated within temperate Matapouri Estuary, northern New Zealand. The density and distribution of fauna were sampled within six distinctive habitats (mangrove stands, pneumatophore zones, Zostera beds, channels, banks, and sand flats), within four sampling events between December 2002 and September 2003. Each type of habitat was replicated seven times within different locations in the estuary. Counts of all infauna and epifauna within four replicate cores were recorded from each habitat and location. Multidimensional scaling plots were used to identify differences in structure and composition of assemblages among habitats and locations within each sampling event. Results from these benthic samples indicate that Matapouri Estuary has a high overall biodiversity, with distinctive faunal assemblages found within different habitats, and some seasonal variations also apparent. In terms of both number of individuals and taxa per unit area, seagrass beds had the highest numbers and mangrove areas had the lowest numbers, with all other habitats in between. Some locations were found to support a high diversity of organisms across habitats, while other locations had high densities of a few species only. Several physical and biological differences between tropical/sub-tropical and New Zealand’s temperate mangrove habitats are put forth as potential reasons for the lower density and diversity of the benthic component observed herein. Further ongoing studies aim to elucidate the structure and interactions within food webs in this estuarine ecosystem. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: benthic fauna; estuarine habitats; mangroves; seagrass; sand flats; biodiversity

1. Introduction The complex dynamics that exist within biologically rich habitats, such as mangroves and seagrasses, have received considerable attention in the past (see overviews in Hemminga and Duarte, 2000; Hogarth, 2000). Seagrass beds have been identified as one of the most productive areas in the oceans, with various trophic levels, and complex species-dominance structures and succession patterns (Bell and Westoby, 1986; Edgar, 1990; Turner et al., 1999; Hughes et al., 2004; van Houte-Howes

E-mail address: [email protected] 0272-7714/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2005.07.024

et al., 2004). In New Zealand, van Houte-Howes et al. (2004) observed significant differences in benthic community composition inside and outside seagrass areas within three estuaries, owing to small changes in the relative abundance of dominant taxa. However, seagrass beds did not always have the highest biodiversity, abundance, or biomass compared to adjacent unvegetated areas. Furthermore, boundaries between these habitats appeared to have distinctive community compositions, thus illustrating the importance of inter-habitat interactions and complexity within these estuaries. Sandy shores also have been investigated for their contribution to the overall biodiversity and species composition of estuaries in New Zealand (Turner et al., 1995, 1997; Hewitt et al., 1997; Whitlatch et al.,

98

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

1997). Turner et al. (1997) investigated the effect of bivalve post-settlement transport and deposition on the spatial distribution and density of bivalves in intertidal sand flats in the Manukau Harbour, New Zealand. Numerous studies on mangrove habitats have demonstrated the high biological productivity and rich biodiversity of these ecosystems in tropical and sub-tropical regions (Lindegarth and Hoskin, 2001; Valiela et al., 2001; Ashton and Macintosh, 2002; Macintosh et al., 2002). Such studies also have highlighted the threats to these fragile ecosystems, caused by mangrove removal for shrimp farms, salt ponds, wood and pulp production, and other human activities (Laegdsgaard and Johnston, 2001; Valiela et al., 2001; Diop, 2003). Unlike mangrove stands in tropical and sub-tropical areas of the world, New Zealand mangroves are not displaced for aquaculture farms or wood products, but may be reclaimed for livestock grazing, and dumping of waste products (Woodroffe, 1982, 1985; Young and Harvey, 1996). Moreover, the natural process of estuarine in-filling in New Zealand has been enhanced, in many cases, by catchment-derived human impacts resulting from land clearance and development (Hume and Dahm, 1992). These changes increase sediment loads downstream, which favor mangrove colonization and expansion (Woodroffe, 1982, 1985; Young and Harvey, 1996). While these mangrove habitats continue to spread, they often overtake adjacent habitats (i.e., sand flats, seagrass beds, marshland). These often dramatic changes in estuarine physiography have led to various management strategies. As a result, some community groups question whether New Zealand mangrove ecosystems are as productive and diverse as the overseas examples, and whether they deserve protection status. Benthic community composition studies in New Zealand mangrove environments have reported on a host of infauna and epifauna, which although not restricted to these habitats, are likely to be important components of estuarine food webs and trophic dynamics (May, 1999; Morrisey et al., 2002; Ellis et al., 2004). Furthermore, comparative studies within mangrove stands have revealed differences in benthic biomass and diversity associated with the age of the mangroves (Morrisey et al., 2002). Ellis et al. (2004) identified differences in macro-benthic communities between mangrove and non-vegetated estuarine habitats. While these studies provide initial evidence that different habitats may contribute differentially to the biodiversity and food webs of temperate estuaries, to date, there has been insufficient research to enable scientists and managers to assess the ecological value of these ecosystems, and to predict the potential effects of mangrove expansions on adjacent habitats in New Zealand. Baseline information, monitoring programs, and experimental trials are needed before adequate assessment can be made of the ecological value of New Zealand’s temperate mangroves. The aim of this research was to quantify and compare the composition of benthic macro-fauna within distinctive estuarine habitats (mangrove stands, pneumatophore zones, seagrass beds, channels, banks, and sand flats). It is a first step toward evaluating the relative importance of habitats with different structures and complexities in northern New Zealand estuaries.

2. Methods and materials 2.1. Study site The study site is located at Matapouri Estuary (35  34#S and 174  30#E), about 35 km northeast of Whangarei, northern New Zealand (Fig. 1). Mangroves (Avicennia marina var. australasica) dominate the estuary, but a variety of other habitats can also be found (e.g., seagrass beds, sand flats, salt marsh). Two streams feed into the two major arms of the estuary from different catchments, southerly Parangarau and northerly Te Wairoa (Fig. 1). The estuary is tidally dominated (M2 tidal period) with little freshwater influence (Hume and Herdendorf, 1988). The combined catchment area is about 3000 m2, with a highest altitude of 209 m. The estuary itself covers approximately 72 ha with a narrow opening to Matapouri Bay and the open ocean (Fig. 1). A variety of habitats and relatively high species diversity make this estuary an ideal site to investigate benthic community structure across different habitat gradients. Seven locations were identified along each of the two arms of the estuary, proximally and distally from the mouth of the estuary (Fig. 1). Within each location, a transect line was placed across the channel and adjacent high ground areas. The transect lines incorporated several distinctive habitats, based on vegetation type, sediment characteristics, and tidal inundation. The transect line was used as a reference point to locate random points within each habitat where samples were taken. A new set of random points was selected for each sampling date. However, not all habitats were represented in all locations, and some habitats were found repeated on the other side of the channel within the same location (Fig. 1). The major habitats are characterized as: Mangrove habitat (M): mangrove stands (Avicennia marina var. australasica) of similar height (w3e4 m), density (w10/5 m2), and dense canopy cover (between 50 and 90%) are found within each of the two estuarine arms. The sediment of mangrove habitats along both channels mostly is muddy, with dense fibrous root mats just below the surface to about 20 cm depth. Pneumatophore habitat (P): mangrove aerial roots are found in high density (up to 200/m2) in the mangrove fringe, within soft mud at the edge of the channels. The density of pneumatophores within each location may vary from 80 to 200/m2 and, in some cases, loose-lying algal mats, especially Hormosira banksii, may be found in high numbers among pneumatophores. Pneumatophores of up to 50 cm in above-ground length are predominant, and often are covered with barnacles, oysters, and mussels. Seagrass bed habitat (Z): distinctive patches of seagrass, Zostera capricorni, are found along both arms of the estuary within sandy/muddy substrates. The seagrass blades may be long (up to 30 cm in length) in the summer, and often are shorter (!1 cm) in winter and after strong storms. Loose-lying algal mats may also be found in these habitats. Channel habitat (C): both main channels at Matapouri tend to have gravelly/sandy bottoms. Main and secondary

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

99

Fig. 1. Map of the study site at Matapouri Estuary, northern New Zealand. Transect lines are shown within seven locations across various sampling habitats.

channels are well-defined at low tide, but are inundated, often beyond recognition, at high tide. At the lowest tide, the deepest parts of the channels may drain to about 1 m water depth. The channels are strongly influenced by both freshwater and saltwater inputs throughout the estuary. Bank habitat (B): a gravelly/shelly bank habitat between the sand flat and channel was included in this study because pilot work indicated that these areas contained distinctive faunal compositions. The slope within these habitats varies from about 20  to 60  at the edge of the channel. Sand flat habitat (S): fluffy, coarse sand is found primarily near the mouth of the estuary. This area has a very shallow slope, and is inundated quickly when the tide comes in. The sand compaction in this habitat is very low, and forms a well-aerated sedimentary environment.

2.2. Sampling Vegetation/algal surveys were conducted during each sampling event (December 2002, March, June, and August 2003) in mangrove, pneumatophore, and seagrass bed habitats. Within mangrove habitats, the densities were recorded of mangrove trees (taller than 0.5 m, and more than 2.5 cm in stem diameter) and seedlings (taller than 0.5 m, but less than 2.5 cm in stem diameter) within five 5-m2 quadrats. In addition, the mean height and diameter at breast height (dbh) of 10 random mangrove trees, anywhere in the habitat, also were recorded. The density of mangrove seedlings (shorter than 0.5 m), propagules (dispersing seedling of about 3 cm in diameter) and pneumatophores in mangrove and pneumatophore habitats was determined using five replicate quadrats of a 0.25 m2

100

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

area. The percent mangrove leaf litter was estimated inside each of five 0.25 m2 quadrats within mangrove and pneumatophore habitats. Five 0.25 m2 quadrats also were used to estimate algal (Hormosira banksii) density in pneumatophore and seagrass bed habitats. Two replicate sediment samples (15 ! 15 ! 15 cm) were taken from each habitat and location during each sampling event (December 2002, March, June, and August 2003) for grain size analysis and to determine organic content. Grain size characterization was achieved by passing each sample through several sieves of different mesh sizes (coarse sand Z O600 mm, medium sand Z 300e600 mm, fine sand Z 150e300 mm, and mud Z !150 mm), and calculating the percent contribution of each sediment category. Measurements of total organic carbon were obtained through weight differences before and after total combustion of the samples in a furnace at 450  C after acidification to a pH of 2 (Parrish, 1998). Measurements of sediment compaction within each habitat were obtained by recording the depth of penetration of a sharpened steel rod (50 cm in length, 0.7 cm in diameter, and 150 g weight) when dropped from a distance of 1.2 m above the sediment surface (Morrisey et al., 2002). Measurements of water temperature, salinity, dissolved oxygen, and tidal inundation were recorded simultaneously in the channel habitats at each of the seven sampling locations to identity relative differences among locations during each sampling event. Benthic fauna were sampled in December 2002, March, June, and August 2003. Four replicate 15 ! 15 ! 15 cm sediment cores were sampled for epifauna and infauna within each habitat at each location. The cores were taken from random points throughout each habitat, using the transect line as a reference point. All samples were sieved through a 0.5 mm mesh. Counts of all fauna and maximum lengths of the dominant bivalves were recorded, following species identification to the lowest possible taxonomic level. In most cases, the lowest taxonomic level was species or genus, but identification of oligochaete and polychaete worms was only possible to family level. Although the use of different taxonomic levels, and especially broad classifications, may result in some loss of information and ability to distinguish differences among habitats, these effects have been shown to have little impact on spatial and temporal variability in assemblages of macro-fauna (James et al., 1995; Olsgard et al., 1997; Chapman, 1998; Lindegarth and Hoskin, 2001). Statistical analyses to determine differences in faunal composition and sediment characteristics among habitats, locations, and dates involved a nested three-factor ANOVA, with date and location as fixed factors, and habitat nested within location as a random factor. Data that did not meet the requirements for parametric analyses were transformed with an arcsine or a squared root of x C 0.5 transformation to meet these requirements. Plant characteristics were analyzed with a two-factor ANOVA. Principal Components Analysis (PCA) was used to detect habitat differences, based on sediment and vegetation/algal characteristics. Multiple Dimension Scaling (MDS) plots were constructed, based on similarities of

correlation matrices, to detect groupings of faunal assemblages and habitat types. Statistica and Minitab software were used for statistical analyses. 3. Results 3.1. Environmental parameters The physical parameters were similar within the Parangarau and Te Wairoa channels throughout the experimental period, indicating the well-mixed nature of this estuary. Water temperature ranged from 9.3 to 12.5  C in winter and 12.8 to 14.1  C in summer. Salinity and dissolved oxygen measurements were taken during high tide at the sampling locations throughout the study period, and these measurements ranged from 8.6 to 31.3& and 7.1 to 10.2 mg/L, respectively. The range in these parameters reflects the strong influence of freshwater and saltwater inputs in this tidally driven estuary. The level of tidal inundation varied among habitats, but these differences were consistent among the seven locations. Mangrove stands always had the highest elevation. Other habitats had tidal inundations of about ÿ0.3 m (pneumatophore zone), ÿ0.52 m (seagrass beds), ÿ0.74 (banks), and ÿ1.1 m (channels’ edge) relative to mangrove stands. 3.2. Vegetation/algae Results from vegetation and algal parameters within mangrove, pneumatophore, and seagrass habitats at the five locations where these habitats were present are reported in Table 1. Mangrove habitats on the southern stream (locations 6 and 7) were characterized as younger stands with shorter and more densely populated trees. Conversely, the northern channel (location 1) had the tallest trees and the lowest density of trees per unit area. As expected, these tree patterns were consistent among dates. Two-factor ANOVAs resulted in significant differences ( p ! 0.001) among locations for the number of trees, tree height, dbh, number of saplings and seedlings within mangrove and pneumatophore habitats. The younger mangrove stands in locations 6 and 7 also had the highest number of saplings and seedlings of all mangrove habitats (Table 1). The densities of propagules within mangrove, pneumatophore, and seagrass habitats were always significantly different ( p ! 0.001) among sampling dates, locations and interactions, which appears to reflect the random dispersal and retention of these seeds. Pneumatophores were most abundant in mangrove and pneumatophore habitats within locations 1 and 2 ( p O 0.001), and these differences were consistent among sampling dates ( p O 0.001). Leaf litter was found consistently in greater amounts in mangrove and pneumatophore habitats compared to seagrass habitats. In addition, the percent leaf litter did not differ ( p O 0.001) among dates and locations within each of these habitats. Furthermore, drift algae were found in greater quantities in pneumatophore and seagrass habitats compared to mangrove habitats, although there were significant differences among dates and locations ( p ! 0.001) within each habitat. Seagrass cover within the

(1.3) (2.0) (1.7) (1.3) (2.0) 23.1 27.9 21.0 23.7 21.6

e e e e e

e e e e e

sampled quadrats always was 100%. The highest amount (wet weight) of seagrass plants were found in location 2 ( p ! 0.001), and these differences were consistent among sampling dates ( p O 0.001).

(1.8) (4.3) (2.6) (2.8) (4.1) 16.1 27.3 10.9 11.3 14.4 (0.5) (1.2) (1.0) (0.8) (1.1) 1.8 2.6 1.3 1.5 1.3

(1.5) (6.0) (3.9) (3.4) (5.0) 8.4 21.3 14.7 16.9 13.6 (0.7) (0.6) (1.1) (0.4) (0.9) 2.2 2.3 4.2 2.3 2.5

(0.3) (0.6) (0.5) (0.3) (0.6) e e e e e

0.9 1.6 1.9 1.2 0.7

e e e e e

(0.6) (0.8) (0.9) (0.6) (0.9) 10.0 10.4 9.4 9.3 6.5 (0.3) (0.6) (0.3) (0.4) (0.5) (0.2) (0.4) (0.3) (0.2) (0.3) 0.6 1.2 1.2 1.3 2.1

1.0 1.9 0.8 0.3 0.3

(0.3) (0.3) (0.3) (0.3) (0.3)

e e e e e

e e e e e e e e e e

e e e e e

e e e e e

e e e e e

The six habitats were easily separated by their sediment characteristics. Coarse sand was most abundant in the channel habitats, and medium sand was most common in the sand flat and bank habitats (Fig. 2, Table 2). Fine sand was dominant in mangrove and pneumatophore habitats, while mud was abundant in mangrove, pneumatophore, and seagrass habitats (Fig. 1, Table 2). The sediment was least compacted in the sand flat habitats, and most compacted in the mangrove and channel habitats. Organic content was highest in mangrove and seagrass sediments, while channels had the least amount of organic material (Table 2). Separate three-factor nested ANOVAs resulted in non-significant differences ( p O 0.001) among sampling dates, but significant differences ( p ! 0.001) among locations and habitats (locations) for all sediment characteristics. The PCA ordination of sediment and plant characteristics revealed clear habitat clusters, except for seagrass and pneumatophore habitats, which overlapped considerably (Fig. 3). The variable loadings from the principal components 1e3 accounted for 83.8% of the variation (Table 3). Component 1 indicates a high loading from medium sand, and a high negative loading for mud, organic content, and fine sand. Component 2 reflects a coarse sand factor, and a negative penetrometer depth factor. The third component is associated with leaf litter and algal cover. 3.4. Benthic fauna Results from the benthic faunal samples collected within each of four sampling events (December 2002, March, June, and September 2003) indicate a generally consistent pattern among the sampling events (Fig. 4, Table 4). Seagrass beds tended to have the highest total number (GSE) of individuals (267.6 G 33.5 ind./core) and total taxa (135.6 G 15.7 taxa/ core) among all the locations sampled, followed by channel

1 2 5 6 7

1 2 5 6 7

Percent

e e e e e

80

e e e e e

(0.6) (0.5) (1.0) (0.5) (0.2)

Coarse Sand

100

9.9 8.3 9.1 12.2 12.7

4.7 3.8 3.7 4.0 3.6

(0.1) (0.1) (0.2) (0.1) (0.2)

4.4 2.5 3.9 4.4 3.5

(0.1) (0.1) (0.1) (0.2) (0.2)

4.4 2.5 1.8 5.5 5.4

(0.5) (0.6) (0.6) (0.4) (0.3)

0.7 1.1 0.8 2.3 2.4

1.2 3.1 1.2 0.2 0.6

(0.4) (0.9) (0.4) (0.5) (0.7)

11.3 10.8 9.1 8.4 5.5

(0.6) (0.8) (0.8) (0.6) (0.8)

5.4 3.4 6.2 2.6 2.4

(1.1) (0.9) (1.2) (0.6) (1.1)

3.8 9.3 2.0 4.0 3.4

(1.0) (3.4) (0.8) (1.8) (2.6)

3.3. Sediments

1 2 5 6 7

Leaf litter (% cover/0.25 m2) Pneumatophores (#/0.25 m2) Propagules (#/0.25 m2) Seedlings (#/0.25 m2) Saplings (#/5 m2) dbh (cm) Tree height (m) Trees (#/5 m2) Location

101

Medium Sand

Fine Sand

Mud

60 40 20 M

P

Z

C

B

S

Habitat Seagrass

Pneumatophore

Mangrove

0

Habitat

Table 1 Mean (GSE) vegetation and algal measurements within mangrove, pneumatophore, and seagrass habitats, and within five locations at Matapouri Estuary

Algal density (% cover/0.25 m2)

Seagrass (g wet wt.)

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

Fig. 2. Grain size analysis for sediments within various habitats (M Z mangrove, P Z pneumatophore, Z Z seagrass, C Z channel, B Z bank, and S Z sand flat) at Matapouri Estuary.

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

102

Table 2 Mean (GSE) values for sediment characteristics (penetrometer depth, grain size, and organic content) within six habitats (M Z mangrove, P Z pneumatophore, Z Z seagrass, C Z channel, B Z bank, and S Z sand flat) at Matapouri Estuary M

P

3.9 (0.7)

Penetrometer depth (cm) Grain size (%) Course sand (O600 mm) Medium sand (300e600 mm) Fine sand (150e300 mm) Mud (O150 mm) Organic content (%)

0.1 5.0 84.6 10.1 11.4

Z

10.8 (1.5)

(0.1) (2.6) (2.8) (0.4) (1.6)

0.0 26.8 63.4 9.8 8.6

(0.0) (8.8) (8.9) (1.2) (3.5)

habitats, while mangrove habitats always had the lowest number (GSE) of individuals (43.9 G 16.1 ind./core) and taxa (29.4 G 2.7 taxa/core) throughout the sampling period. However, differences among sampling locations were not observed (Table 4). The bivalves, Paphies australis and Austrovenus stutchburyi, were present throughout habitats and locations, but their densities (GSE) varied among habitats (Fig. 5). Paphies australis generally were most common in sand flats (105.6 G 62.5 ind./core) and banks (63.5 G 25.1 ind./core), but their largest sizes were found in the channel (24.6 G 0.9 mm) and bank (15.2 G 3.0 mm) habitats. Juvenile P. australis often were found in large numbers near the water table in some sand flat habitats (Fig. 5). For A. stutchburyi, the highest densities were found in the seagrass beds (116.7 G 65.4 ind./core), where they seem to recruit, and the largest animals were found in mangrove (26.3 G 3.9 mm) and pneumatophore (17.5 G 0.8 mm) habitats (Fig. 5). Crabs and shrimp were most abundant (GSE) in seagrass beds (1.0 G 0.2 and 0.6 G 0.1 ind./core, respectively), followed by channel habitats (0.4 G 0.1 and 0.3 G 0.1 ind./core, respectively) (Fig. 6). Oligochaete worms were present throughout the habitats and locations, but were most abundant (GSE) in channel

3

2

PC1

1

C

6.9 (2.3) 2.1 47.1 38.0 12.7 10.5

(0.4) (3.3) (2.0) (5.3) (3.2)

B

3.2 (0.7) 46.0 30.4 26.4 0.6 1.9

S

4.5 (1.5)

(3.6) (3.1) (5.3) (0.6) (0.4)

0.3 75.4 23.6 0.7 4.2

(0.1) (3.6) (3.3) (0.3) (1.3)

17.3 (2.3) 0.0 87.5 12.4 0.1 3.4

(0.0) (2.5) (2.5) (0.0) (0.8)

(52.4 G 8.7 ind./core) and bank (45.7 G 7.8 ind./core) habitats (Fig. 6). Amphipods were most abundant (GSE) in bank habitats (16.9 G 2.2 ind./core) and generally absent in mangrove, pneumatophore, and seagrass habitats (Fig. 6). Grazing snails (i.e., Turbo smaragdus, Diloma subrostrata, Melagraphia aethiops) were found in high densities (GSE) in seagrass beds (20.1 G 3.0 ind./core), followed by pneumatophore (6.1 G 2.1 ind./core) habitats, while predatory/scavenger snails (i.e., Cominella glandiformis, Zeacumanthus sp., Lepsiella scorbina) were present in higher densities (GSE) in seagrass (24.2 G 1.2 ind./core) and channel (14.7 G 2.3 ind./core) habitats (Fig. 7). Results from multivariate analyses indicate that there were significant differences among sampling dates, habitats within locations, and interactions for most taxa, and no significant differences among locations for all taxa, except P. australis (Table 4). A high number of interactions reflected the patchiness and mobility of some of these benthic populations. The MDS plots revealed a clear separation of taxa (Fig. 8) and habitats (Fig. 9) among sampling dates, which indicate differences in average structure and composition among faunal assemblages in the various habitats. Within all sampling dates, Austrovenus stutchburyi and oligochaete worms clearly separated from other taxa, but sometimes overlapped with one another (Fig. 8). Paphies australis and amphipods also clustered away from other taxa and each other. MDS plots for habitats also revealed similar grouping trends among sampling dates (Fig. 9). All habitats appeared in distinctive groups, except for a slight overlap between mangrove and pneumatophore habitats, and between channel and bank habitats (Fig. 9).

0

-1

Table 3 PCA results showing the first three components for sediment and plant/algal variables within six habitats at Matapouri Estuary

-2

Variable

PC1

PC2

PC3

Coarse sand Medium sand Fine sand Mud Penetrometer Organic content Leaf litter Algal cover

0.284 0.751 ÿ0.856 ÿ0.907 0.367 ÿ0.858 ÿ0.574 ÿ0.672

0.804 ÿ0.550 0.194 ÿ0.105 ÿ0.769 ÿ0.313 ÿ0.197 ÿ0.233

ÿ0.415 ÿ0.238 0.410 0.032 0.117 0.080 ÿ0.629 ÿ0.507

Total variation (%) Cumulative variation (%)

48.2 48.2

22.2 70.4

13.4 83.8

-3 -2

-1

0

1

2

3

PC2 Fig. 3. PCA plot of sediment (percent coarse, medium, and fine sand, mud, organic content, penetrometer depth), and plant (percent leaf litter and algae) variables across six habitats. Habitats are denoted as: mangrove Z solid squares (-), pneumatophore Z solid triangles (:), seagrass Z solid circles (C), channel Z exes (!), bank Z open triangles (O), and sand flat Z open circles (B).

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110 Dec

Jun

Sep

Total individuals

400

Mean Abundance (#/core)

Mar

300

200

100

0 M

Z

C

B

S

Total taxa

30

Mean Abundance (#/core)

P

103

(e.g., Australia, Fiji), and in parts of the sub-topics, to rigorously evaluate the ecological importance of mangrove stands compared to other adjacent habitats, especially in estuaries where mangroves may be expanding. This study provides the first comprehensive investigation of benthic macro-invertebrate community composition within mangrove/seagrass and adjacent settings in a New Zealand estuary, as a step toward a more critical evaluation of these temperate habitats. Results from this research show that the estuarine habitats at Matapouri are clearly distinctive on the basis of vegetation and sediment characteristics. There is greater diversity and density of organisms in seagrass beds and channel habitats. Diversity and density decrease landward toward mangrove habitats, where the lowest values are found. The different habitats appear to provide unique resources that are exploited by different groups of benthic fauna. These unique habitats and their faunal associations are discussed herein. 4.1. Habitat structure

20

10

0 M

P

Z

C

B

S

Habitat Fig. 4. Mean (GSE) number of individuals and taxa within six habitats (M Z mangrove, P Z pneumatophore, Z Z seagrass, C Z channel, B Z bank, and S Z sand flat) at Matapouri Estuary.

The spread of the data and, in some cases, overlap of the groups were strongly influenced by the unusually high organism density and diversity in location 2. The seagrass habitat at this location was consistently rich in organisms, and this effect also was noticed within the adjacent habitats. The range of stress-values was low among the MDS plots for taxa (0.02e 0.05) and habitats (0.07e0.15), which strongly supports the data interpretations (Warwick and Clarke, 1993). 4. Discussion Numerous studies have highlighted the rich biodiversity and ecological importance of mangrove and seagrass habitats throughout the world, including New Zealand. However, few studies have assessed the ecological value of mangrove habitats compared to other estuarine habitats. Such comparisons are generally lacking for temperate New Zealand mangrove ecosystems (but see: Morrisey et al., 2002; Ellis et al., 2004), yet are sorely needed in the current debate regarding mangrove management and conservation. Furthermore, New Zealand mangrove ecosystems may not be unique in their departure from serving as biodiversity-rich habitats or important nursery/feeding ground areas. Further comparative studies are needed in other regions dominated by Avicennia marina

Sediment characteristics alone resulted in clear differences among habitats, except for pneumatophore and seagrass habitats. These sediment differences are of crucial importance for most benthic animals, since their feeding strategies tend to be highly adapted to sediment type (McLachlan et al., 1995; Zhuang and Wang, 2004). In addition, plant structures, such as mangrove trees, pneumatophores, and seagrasses provide important architectures (i.e., settlement and hiding areas) and sources of nutrients for various species (Schrijvers et al., 1995; Gee and Somerfield, 1997; Lee, 1999; Turner et al., 1999; Satumanatpan and Keough, 2001). Generally, it has been shown that structurally complex habitats, such as seagrasses, marshes, and mangroves support higher densities of benthic organisms compared to non-vegetated areas (Kneib, 1984; Orth et al., 1984; Edgar, 1990). In addition to the greater number of settlement sites and enhanced nutrient availability, lower predation pressure has been found within complex architectures (structural refuge) compared to open areas (Kneib, 1984; Summerson and Peterson, 1984; Davis et al., 2001). In this study, mangrove habitats had the highest degree of threedimensional structure, but only a small portion (up to about 1 m above the sediment) was exposed to tidal inundation and accessible to marine invertebrates and fish. In contrast, pneumatophore and seagrass beds provided a higher density of potential invertebrate settling structures, and had longer inundation periods. Sand flats and channels lacked above-ground structures, but provided a dynamic infaunal environment with frequent inundation (i.e., habitat access and food delivery). The amount of organic matter available to marine organisms (on the benthos and within the sediment) was highest within vegetated areas (mangrove, seagrass, and pneumatophore habitats), although it is difficult to ascertain what proportion of these nutrients is consumed by organisms in these areas versus exported to other habitats. Many studies have investigated direct and indirect nutrient flow-on effects on faunal composition within vegetated estuarine environments (Duarte, 1995; Valiela et al., 1997; Dittmar et al., 2001; Macintosh et al.,

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

104

Table 4 Statistical analyses (nested three-factor ANOVA) for macro-fauna within six habitats, seven locations, and during four sampling dates. Significant tests are in bold F

p

df

MS

82.71 0.77 6.08 55.58

0.001 0.600 0.001 0.001

Total taxa 3 6 18 25 619

854.96 1138.33 79.65 945.99 19.84

164.83 5.48 7.10 24.10

0.001 0.001 0.001 0.001

3.02 4.45 0.32 3.92 0.14

20.96 1.10 2.22 27.26

4.77 12.46 2.99 77.83 1.516

Source

df

MS

Date Location Date ! location Habitat (location) Error

Total individuals 3 167 489 6 90 045 18 12 314 25 112 539 619 2025

Date Location Date ! location Habitat (location) Error

Paphies australis 3 416.33 6 346.06 18 17.94 25 60.87 619 2.53

Date Location Date ! location Habitat (location) Error

Crabs 3 6 18 25 619

Date Location Date ! location Habitat (location) Error

Oligochaetes 3 6 18 25 619

Date Location Date ! location Habitat (location) Error

Herbivorous snails 3 1.60 6 33.91 18 0.76 25 39.88 619 0.307

F

p

43.08 1.16 4.01 47.67

0.001 0.358 0.001 0.001

Austrovenus stutchburyi 3 172.63 6 65.28 18 10.45 25 136.06 619 2.504

68.94 0.46 4.17 54.33

0.001 0.829 0.001 0.001

0.001 0.393 0.001 0.001

Shrimp 3 6 18 25 619

14.48 0.83 1.52 20.30

0.001 0.555 0.077 0.001

3.15 0.15 1.98 51.33

0.025 0.986 0.009 0.001

Amphipods 3 6 18 25 619

2.40 3.51 1.60 60.31

0.067 0.012 0.056 0.001

5.23 0.82 2.48 129.81

0.001 0.565 0.001 0.001

Scavenger snails 3 1.90 6 50.28 18 0.84 25 52.88 619 0.364

5.23 0.92 2.32 145.38

0.001 0.500 0.002 0.001

2002; Hughes et al., 2004). From this body of literature, it is apparent that complex, ‘‘top-down’’ predator and grazing effects and ‘‘bottom-up’’ nutrient effects on vegetative biomass both enhance the ecological value of these environments (Valiela et al., 2001; Hughes et al., 2004). The present study provides preliminary information regarding the major biological and physical components within vegetated and un-vegetated habitats. Nonetheless, further investigations are needed to elucidate trophic complexities and cascading effects before the importance of habitat structure on faunal composition can be ascertained in Matapouri Estuary and other New Zealand estuaries. 4.2. Faunal composition Results from the faunal composition analyses indicate that mangrove habitats have the lowest density and biodiversity among the six habitats studied at Matapouri Estuary. Conversely, seagrass beds had the highest number of individuals and taxa. Comparisons of benthic organisms between mangrove, seagrass, and non-vegetated habitats in other estuarine systems throughout the world report mixed results (Wells, 1983, 1986; Edgar, 1990; Sheridan, 1997; Ellis et al., 2004). In the tropics, Kolehmainen and Hildner (1975) found that mangrove areas in a Puerto Rican swamp had 6e60 times

1.53 1.8582 0.16 2.15 0.11 0.97 88.85 0.64 24.37 0.404

higher benthic biomass than adjacent seagrasses, while Sheridan (1997) reported higher benthic population densities in mangrove habitats compared to adjacent seagrass and nonvegetated areas in Rookery Bay, Florida, although overall biodiversity was higher in seagrass beds. In temperate New Zealand, Ellis et al. (2004) found lower diversity and density of macro-fauna in mangrove habitats compared to sand flat areas, and slightly lower values than in adjacent mudflats. These differences were suggested to be a result of increased silt/clay sedimentation within mangrove habitats in the Mangemangeroa and Waikopua estuaries (Ellis et al., 2004). Direct comparisons among studies are difficult, owing to variations in sampling methodologies. However, the faunal densities in mangrove habitats found in this study (about 8000 ind./m2) are much lower than those found by Sheridan (1997) (about 38,000 ind./m2) in a similar study in Rookery Bay, Florida. Schrijvers et al. (1998) also found higher densities of benthic fauna (about 23,000 ind./m2) in mangrove areas in Gazi Bay, southern Kenya. However, two New Zealand studies reported similarly low densities of about 6000 ind./m2 (Morrisey et al., 2002) and 1600 ind./m2 (Ellis et al., 2004) in mangrove stands. Within this study, the six vegetated and un-vegetated habitats separated well within the MDS plot containing the main faunal groups found throughout the estuary. These distinct

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110 Dec P. australis

Mean Abundance (#/core)

200

150

100

100

50

50

Sep A. stutchburyi

0 M

P

Z

C

B

S

M

P. australis

30

20

10

10

M

P

Z

C

B

P

Z

C

0

S

B

S

A. stutchburyi

30

20

0

Jun

200

150

0

Mean Shell Length (cm)

Mar

105

M

P

Z

C

B

S

Habitat Fig. 5. Mean (GSE) abundance and shell length for two common bivalves (Paphies australis and Austrovenus stutchburyi) within six habitats (M Z mangrove, P Z pneumatophore, Z Z seagrass, C Z channel, B Z bank, and S Z sand flat) at Matapouri Estuary.

Dec Crabs

Mean Abundance (#/core)

1.5

Jun

50

0.5

25

M

P

Z

C

B

S

Shrimp

1.5

0

Sep Oligochaetes

75

1

0

Mean Abundance (#/core)

Mar

M

P

Z

C

B

S

C

B

S

Amphipods

25 20

1

15 10

0.5

5 0 M

P

Z

C

B

S

0 M

P

Z

Habitat Fig. 6. Mean (GSE) abundance of crabs, shrimp, oligochaetes and amphipods within six habitats (M Z mangrove, P Z pneumatophore, Z Z seagrass, C Z channel, B Z bank, and S Z sand flat) at Matapouri Estuary.

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

106

Mar

Dec

Jun

Grazing snails

25

Mean Abundance (#/core)

Sep

20 15 10 5 0 M

P

Z

C

S

Predatory/Scavenger snails

25

Mean Abundance (#/core)

B

20 15 10 5 0 M

P

C

Z

B

S

Habitat Fig. 7. Mean (GSE) abundance of grazing snails and predatory/scavenger snails within six habitats (M Z mangrove, P Z pneumatophore, Z Z seagrass, C Z channel, B Z bank, and S Z sand flat) at Matapouri Estuary.

differences suggest that, although some animals may be found throughout all habitats (i.e., Austrovenus stutchburyi and Paphies australis), most groups (except for annelids) tend to dominate in one particular habitat. Furthermore, distinctive faunal assemblages were found within different habitats, and the abundances of dominant taxa were generally consistent among sampling events. Seagrass beds appear to provide good feeding and hiding grounds for organisms within a wide range of functional groups, including deposit feeders, scavengers, grazers, and predators. The presence of high numbers of juvenile bivalves and snails also indicates that these areas are good nursery grounds. Crabs and shrimp were prominent in seagrass beds, and adjacent channels and pneumatophore habitats. These mobile invertebrates are highly selective to dense seagrass cover, where they feed on a variety of meiofauna (Bell and Westoby, 1986; May, 1999). Small fish, and larger eels, and flounder were observed feeding in these areas throughout the study period (A. Alfaro, personal observations), although further investigations need to be conducted to elucidate the importance of these temperate estuarine habitats for fish populations. However, these results and observations are consistent with the large body of literature that describes seagrass beds as productive habitats with a high density and diversity of organisms (Edgar, 1990; Connolly, 1997; Nelson and Waaland, 1997; Nagelkerken et al., 2000). By contrast, mangrove habitats at Matapouri mostly appear to favor the venerid bivalve, Austrovenus stutchburyi, and a variety of deposit-feeding annelids. Austrovenus stutchburyi is tolerant to fine sediment, such as that found within mangrove habitats, where it uses its short siphons to feed on suspended particles. Other New Zealand studies have reported the presence of snails, Amphibola crenata and Potamopyrgus

December 2002

March 2003

Stress = 0.05

Stress = 0.02

June 2003

September 2003

Stress = 0.04

Stress = 0.03

Fig. 8. Non-metric MDS plots of faunal assemblages based on six distinctive habitats at Matapouri Estuary. Fauna are denoted as: predatory/scavenger snails Z solid squares (-), grazing snails Z open squares (,), crabs Z solid circles (C), shrimp Z open circles (B), amphipods Z open triangles (O), Paphies australis Z solid triangles (:), Austrovenus stutchburyi Z open diamonds (>), oligochaetes Z pluses (C).

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

December 2002

March 2003

Stress = 0.07

Stress = 0.09

June 2003

September 2003

Stress = 0.08

Stress = 0.15

107

Fig. 9. Non-metric MDS plots of habitats based on faunal assemblages at Matapouri Estuary. Habitats are denoted as: mangrove Z solid squares (-), pneumatophore Z solid triangles (:), seagrass Z solid circles (C), channel Z exes (!), bank Z open triangles (O, and sand flat Z open circles (B).

antipodarum (sometimes in high abundance), and the mud crab, Helice crassa, within mangrove areas (May, 1999; Morrisey et al., 2002; Ellis et al., 2004). At Matapouri, A. crenata and P. antipodarum are absent in most of the estuary, and are found only in marsh areas adjacent to the catchment (outside the study area). Surprisingly, H. crassa was found in low numbers within Matapouri mangrove habitats, but they were the main crab species within seagrass beds. Helice crassa is a common estuarine crab that constructs burrows in mudflats, and can survive well above the high tide mark among mangroves (Williams et al., 1985; Morrisey et al., 1999). However, its distribution within seagrass beds is poorly known. Faunal composition within pneumatophore zones indicates that these habitats are important ecological transition environments between seagrasses and mangroves. The three-dimensional settlement structures that aerial roots provide and the more sandier sediment characteristics (compared to mangrove habitats), appear to promote relatively high faunal density and diversity. In addition, pneumatophores tend to trap high densities of drift algae (up to 100% cover), especially the resident floating alga, Hormosira banksii, which provides feeding grounds for a variety of snails (i.e., Turbo smaragdus, Diloma subrostrata, Melagraphia aethiops) and other invertebrates (A. Alfaro, personal observations). This algal cover tends to persist over tidal cycles, and may provide a constant supply of nutrients to associated organisms. Although sand flats had high densities of bivalves and amphipods, the overall diversity within these habitats was relatively low. Comparatively higher diversities were found in bank and channel habitats. The suspension-feeding bivalve, Paphies australis, dominated the sand flat habitats, with juveniles aggregated along the freshwater table mark, especially after spawning periods (Austral spring and summer). However, the larger individuals of this species were found in subtidal

channels and adjacent banks. This distribution pattern is consistent with other studies (Hooker, 1995), and supports the notion that this species requires coarse sedimentary environments where their filtration mechanism is less likely to be clogged with fine inorganic particles (Brown, 1983; McLachlan et al., 1995). Thus, organisms in sandy habitats may be more dependent on the delivery of food particles by tidal waters, while the organic matter production of seagrass and pneumatophore habitats appears to sustain resident and transient organisms. 4.3. Mangrove habitats While tropical and sub-tropical mangrove habitats generally are regarded as highly valuable ecological areas that support a high diversity and abundance of organisms, initial reports on temperate New Zealand mangroves have found lower faunal densities than expected (Alfaro, 2004; Ellis et al., 2004). In addition, the present contribution suggests that mangrove habitats support a lower density and diversity of benthic fauna compared to adjacent estuarine habitats. There are several potential physical and biological differences between tropical/ sub-tropical and temperate mangroves that may make extrapolations of studies inappropriate from one region to another. New Zealand mangroves have experienced a dramatic increase in abundance due to catchment clearance of vegetation and human development (Ellis et al., 2004), which in turn have caused accelerated sedimentation rates within estuaries. Increased sedimentation within mangrove habitats has been reported to result in negative functional and structural effects on benthic communities (Ellis et al., 2004). In Australia, the high proportion of tannins from mangrove detritus and mud associated with mangrove habitats has been suggested to be responsible for lower densities and biodiversity of macro-fauna

108

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

within these habitats (Alongi and Christoffersen, 1992; Lee, 1999; Alongi et al., 2000; Ellis et al., 2004), and also are likely to play a major role in structuring New Zealand mangrove ecosystems. In addition, lower temperatures and lower tidal inundations within New Zealand coastal areas may result in slower organic matter decomposition rates compared to tropical and sub-tropical mangrove ecosystems. Another apparent difference between New Zealand mangrove habitats and tropical counterparts is that tropical mangroves generally support a high abundance and diversity of crab species of different sizes, which often feed on mangrove leaves and detritus (Robertson and Daniel, 1989; McIvor and Smith, 1995; Slim et al., 1997). Conversely, few crab species appear to be associated with New Zealand mangroves. The most common mud crab, Helice crassa, is relatively small (up to 4 cm), and it is likely to have a minimal impact on the nutrient transfer process, from mangroves to the rest of the estuarine ecosystem, since it feeds on microalgae and detritus. In addition, compared to other mangrove genera commonly found in the tropics (i.e., Rhizophora), the only New Zealand mangrove, Avicennia marina, has pneumatophores (aerial roots) instead of adventitious roots. Pneumatophores usually are found in high densities along the mangrove fringe, where they provide extensive surface area for settling and transient organisms within a complex three-dimensional structure. Conversely, inside the mangrove stand, short and sparse aerial roots, and single to branching trunks create a less structurally complex benthic environment, compared to many tropical mangrove forests. These structural differences between tropical and New Zealand’s temperate mangrove habitats also may contribute to the apparent benthic macrofaunal differences. Based on the findings herein, it is likely that the global practice of estuarine restoration and conservation in the tropics, which usually implies re-planting mangrove trees and protecting remaining mangrove stands, may not hold for areas where mangroves are spreading. In New Zealand, estuarine restoration and conservation is beginning to depart from this blanket view, to include the management and control of spreading mangrove habitats. Further comparative studies of temperate and tropical/sub-tropical mangrove ecosystems, and between areas of mangrove spread and recession, will need to be conducted before these ecological differences, and their management implications, can be clearly elucidated. Finally, this study has indicated low density and diversity of macro-fauna within mangrove habitats; however, the role of these habitats as sources of nutrients for adjacent areas, and the use of these areas by fish during high tide are yet to be evaluated for New Zealand estuaries. Furthermore, the interrelations among these clearly distinct habitats, in terms of nutrient cycling and food web dynamics, also requires further investigation. 4.4. Summary The ecological importance of mangrove, seagrass, and other estuarine habitats has been well documented throughout the world. Mangrove stands in tropical and sub-tropical regions

are regarded as highly productive ecosystems that support a rich diversity of organisms and provide important nursery habitats. Seagrass beds also have been described as crucial sources of nutrients that maintain a high degree of secondary productivity in the coastal areas they inhabit. In northern New Zealand, mangrove and seagrass habitats often are found in estuaries, but their ecological importance is poorly understood, and has been debated in recent years. The characterization of faunal assemblages within mangrove stands and adjacent estuarine habitats (i.e., seagrass beds, pneumatophore zones, channels, banks, and sand flats) at Matapouri, northern New Zealand, indicate that while seagrasses yield a high density and diversity of macro-fauna, mangrove habitats have the lowest densities and diversities of all the habitats studied. The lower benthic components within New Zealand’s temperate mangroves may be related to sediment loads, tannin concentrations, lack of structural complexity, degree of mangrove vegetation consumption and decomposition, and tidal inundation. Future comparative ecological studies, between temperate and tropical/sub-tropical mangrove stands of the same species, are likely to provide further insights regarding these regional differences.

Acknowledgements This research would not have been possible without the patience and tenacity of numerous field and laboratory assistants from the Auckland University of Technology throughout the study period, including S. Pohe, R. Tana, M. McDowell, A. Goldsmith, E. Beatson, P. Conway, C. Barnaby, N. Soliman, O. Hirad, A. Elian, B. Maxwell, and R. Painter. Technical and editorial assistance were provided by K. Campbell, L. Zemke-White, N. Bennie, and L. Sergent. Comments from two anonymous reviewers improved the manuscript. Special thanks to the Division of Applied Sciences technical staff, C. Silvester and C. Whyburd. Finally, I extend my warm thanks to the community of Matapouri, who supported this project from the start, especially T. Graham, E. Kahn, kaitiaki V. McMath and the Hapu Ngati Rehua, Ngati Wai. Kia ora koutou!

References Alfaro, A.C., 2004. Benthic ecology across habitats in Mangawhai Harbour, northern New Zealand. Technical Report, Northland Regional Council, 33 pp. Alongi, D.M., Christoffersen, P., 1992. Benthic infauna and organismesediment relations in a shallow, tropical coastal area: influence of outwelled mangrove detritus and physical disturbance. Marine Ecology Progress Series 81, 229e245. Alongi, D.M., Tirendi, F., Clough, B.F., 2000. Below-ground decomposition of organic matter in forests of the mangroves Rhizophora stylosa and Avicennia marina along the arid coast of Western Australia. Aquatic Botany 68, 97e122. Ashton, E.C., Macintosh, D.J., 2002. Preliminary assessment of the plant diversity and community ecology of the Sematan mangrove forest, Sarawak, Malaysia. Forest Ecology and Management 166, 111e129.

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110 Bell, J.D., Westoby, M., 1986. Abundance of macrofauna in dense seagrass is due to habitat preference, not predation. Oecologia 68, 205e209. Brown, A.C., 1983. The ecophysiology of sandy beach animals. In: McLachlan, A., Erasmus, T. (Eds.), Sandy Beaches as Ecosystems, pp. 575e603 (The Hague). Chapman, M.G., 1998. Relationships between spatial patterns of benthic assemblages in a mangrove forest using different levels of taxonomic resolution. Marine Ecology Progress Series 162, 71e78. Connolly, R.M., 1997. Differences in composition of small, motile invertebrate assemblages from seagrass and unvegetated habitats in a southern Australian estuary. Hydrobiologia 346, 137e148. Davis, S., Childers, D., Day, J., Rudnick, D., Sklar, F., 2001. Nutrient dynamics in vegetated and unvegetated areas of a southern Everglades mangrove creek. Estuarine, Coastal and Shelf Science 52, 753e768. Diop, S., 2003. Vulnerability assessment of mangroves to environmental change. Estuarine, Coastal and Shelf Science 58, 1e2. Dittmar, T., Lara, R., Kattner, G., 2001. River or mangrove? Tracing major organic matter sources in tropical Brazilian coastal waters. Marine Chemistry 73, 253e271. Duarte, C.M., 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41, 87e112. Edgar, G.J., 1990. The influence of plant structure on the species richness, biomass and secondary production of macrofaunal assemblages associated with Western Australian seagrass beds. Journal of Experimental Marine Biology and Ecology 137, 215e240. Ellis, J., Nicholls, P., Craggs, R., Hofstra, D., Hewitt, J., 2004. Effects of terrigenous sedimentation on mangrove physiology and associated macrobenthic communities. Marine Ecology Progress Series 207, 71e82. Gee, J.M., Somerfield, P.J., 1997. Do mangrove diversity and leaf litter decay promote meiofaunal diversity? Journal of Experimental Marine Biology and Ecology 218, 13e33. Hemminga, M.A., Duarte, C.M., 2000. Seagrass Ecology. Cambridge University Press, Cambridge, UK, 298 pp. Hewitt, J.E., Legendre, P., McArdle, B.H., Thrush, S.F., Bellehumeur, C., Lawrie, S.M., 1997. Identifying relationships between adult and juvenile bivalves at different spatial scales. Journal of Experimental Marine Biology and Ecology 216, 77e98. Hogarth, P., 2000. Biology of Mangroves. Cambridge University Press, Cambridge, UK, 240 pp. Hooker, S.H., 1995. Life history and demography of the pipi, Paphies australis (Bivalvia: Mesodesmatidae) in northeastern New Zealand. Masters Thesis, University of Auckland, New Zealand, 231 pp. Hughes, A.R., Bando, K.J., Rodriguez, L.F., Williams, S.L., 2004. Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach. Marine Ecology Progress Series 282, 87e99. Hume, T.M., Dahm, J., 1992. An Investigation of the Effects of Polynesian and European Land Use on Sedimentation in Coromandel Estuaries (Consultancy Report No. 6104). Department of Conservation, Hamilton Regional Office, Hamilton, New Zealand, 56 pp. Hume, T.M., Herdendorf, C.E., 1988. A geomorphic classification of estuaries and its application to coastal resource management: a New Zealand example. Ocean and Shoreline Management 11, 249e274. van Houte-Howes, S.S., Turner, S.J., Pilditch, C.A., 2004. Spatial differences in macroinvertebrate communities in intertidal seagrass habitats and unvegetated sediment in three New Zealand estuaries. Estuaries 27, 945e957. James, R.J., Lincoln Smith, M.P., Fairweather, P.G., 1995. Sieve mesh-size and taxonomic resolution needed to describe natural spatial variation of marine macrofauna. Marine Ecology Progress Series 118, 187e198. Kneib, R.T., 1984. Patterns of invertebrate distribution and abundance in the intertidal salt marsh: causes and questions. Estuaries 7, 392e412. Kolehmainen, S.E., Hildner, W.K., 1975. Zonation of organisms in Puerto Rican red mangrove (Rhizophora mangle L.) swamps. In: Walsh, G.E., Snedaker, S.C., Teas, H.J. (Eds.), Proceedings of the International Symposium on Biology and Management of Mangroves, pp. 357e369 (Gainesville, Florida). Laegdsgaard, P., Johnston, C., 2001. Why do juvenile fish utilise mangrove habitats? Journal of Experimental Marine Biology and Ecology 257, 229e253.

109

Lee, S.Y., 1999. Tropical mangrove ecology: physical and biotic factors influencing ecosystem structure and function. Australian Journal of Ecology 24, 355e366. Lindegarth, M., Hoskin, M., 2001. Patterns of distribution of macro-fauna in different types of estuarine, soft sediment habitats adjacent to urban and non-urban areas. Estuarine, Coastal and Shelf Science 52, 237e247. Macintosh, D.J., Ashton, E.C., Havanon, S., 2002. Mangrove rehabilitation and intertidal biodiversity: a study in the Ranong mangrove ecosystem, Thailand. Estuarine, Coastal and Shelf Science 55, 331e345. May, J., 1999. Spatial variation in litter production by the mangrove Avicennia marina var. australasica in Rangaunu Harbour, Northland, New Zealand. New Zealand Journal of Marine and Freshwater Research 33, 163e172. McIvor, C.C., Smith III, T.J., 1995. Differences in the crab fauna of mangrove areas at a Southwest Florida and Northeast Australia location: implications for leaf litter processing. Estuaries 18, 591e597. McLachlan, A., Jaramillo, E., Defeo, O., Dugan, J., Ruyck, A., Coetzee, P., 1995. Adaptation of bivalves to different beach types. Journal of Experimental Marine Biology and Ecology 187, 147e160. Morrisey, D.J., DeWitt, T.H., Roper, D.S., Williamson, R.B., 1999. Variations in the depth and morphology of burrows of the mud crab Helice crassa among different types of intertidal sediments in New Zealand. Marine Ecology Progress Series 182, 231e242. Morrisey, D.J., Skilleter, G.A., Ellis, J.I., Burns, B.R., Kemp, C.E., Burt, K., 2002. Differences in benthic fauna and sediment among mangrove (Avicennia marina var. australasica) stands of different ages in New Zealand. Estuarine, Coastal and Shelf Science 56, 581e592. Nagelkerken, I., van der Velde, G., Gorissen, M.W., Meijer, G.J., van’t Hof, T., den Hartog, C., 2000. Importance of mangrove, seagrass beds, and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique. Estuarine, Coastal and Shelf Science 51, 31e44. Nelson, T.A., Waaland, J.R., 1997. Seasonality of eelgrass, epiphyte, and grazer biomass and productivity in subtidal eelgrass meadows subject to moderate tidal amplitude. Aquatic Botany 56, 51e74. Olsgard, F., Somerfield, P.J., Carr, M.R., 1997. Relationships between taxonomic resolution and data transformations in analyses along an established pollution gradient. Marine Ecology Progress Series 149, 173e181. Orth, R.J., Heck Jr., K.L., Van Montfrans, J., 1984. Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predatoreprey relationships. Estuaries 7, 339e350. Parrish, C., 1998. Lipid biogeochemistry of plankton, settling matter and sediments in Trinity Bay, Newfoundland. I. Lipid classes. Organic Geochemistry 29, 1531e1545. Robertson, A.I., Daniel, P.A., 1989. The influence of crabs on litter processing in high intertidal mangrove forests in tropical Australia. Oecologia 78, 191e198. Satumanatpan, S., Keough, M., 2001. Role of larval supply and behavior in determining settlement of barnacles in a temperate mangrove forest. Journal of Experimental Marine Biology and Ecology 260, 133e153. Schrijvers, J., Van Gansbeke, D., Vincx, M., 1995. Macrobenthic infauna of mangroves and surrounding beaches at Gazi Bay, Kenya. Hydrobiologia 306, 53e66. Schrijvers, J., Camargo, M.G., Pratiwi, R., Vincx, M., 1998. The infaunal macrobenthos under East African Ceriops tagal mangroves impacted by epibenthos. Journal of Experimental Marine Biology and Ecology 222, 175e193. Sheridan, P., 1997. Benthos of adjacent mangrove, seagrass and non-vegetated habitats in Rookery Bay, Florida, USA. Estuarine, Coastal and Shelf Science 44, 455e469. Slim, F.J., Hemminga, M.A., Ochieng, C., Jannink, N.T., Cocheret de la Morinie`re, E., van dre Velde, G., 1997. Leaf litter removal by the snail Terebralia palustris (Linnaeus) and sesarmid crabs in an East African mangrove forest (Gazi Bay, Kenya). Journal of Experimental Marine Biology and Ecology 215, 35e48. Summerson, H.C., Peterson, C.H., 1984. Role of predation in organizing benthic communities of a temperate-zone seagrass bed. Marine Ecology Progress Series 15, 63e77.

110

A.C. Alfaro / Estuarine, Coastal and Shelf Science 66 (2006) 97e110

Turner, S.J., Thrush, S.F., Pridmore, R.D., Hewitt, J.E., Cummings, V.J., Maskery, M., 1995. Are soft-sediment communities stable? An example from a windy harbour. Marine Ecology Progress Series 120, 219e230. Turner, S.J., Hewitt, J.E., Wilkinson, M.R., Morrisey, D.J., Thrush, S.F., Cummings, V.J., Funnell, G., 1999. Seagrass patches and landscapes: the influence of wind-wave dynamics and hierarchical arrangements of spatial structure on macrofaunal seagrass communities. Estuaries 22, 1016e1032. Turner, S.J., Grant, J., Hewitt, J.E., Wilkinson, M.R., Hume, T.M., Morrisey, D.J., 1997. Bedload and water-column transport and colonization processes by post-settlement benthic macrofauna: does infaunal density matter? Journal of Experimental Marine Biology and Ecology 216, 51e75. Valiela, I., McClelland, J., Hauxwell, J., Behr, P.J., Hersh, D., Foreman, K., 1997. Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnology and Oceanography 42, 1105e1118. Valiela, I., Bowen, J.L., York, J.K., 2001. Mangrove forests: one of the world’s threatened major tropical environments. BioScience 51, 807e815. Warwick, R.M., Clarke, K.R., 1993. Comparing the severity of disturbance: a meta-analysis of marine macrobenthic community data. Marine Ecology Progress Series 92, 221e231. Wells, F.E., 1983. An analysis of marine invertebrate distributions in a mangrove swamp in northwestern Australia. Bulletin of Marine Science 33, 736e744.

Wells, F.E., 1986. Distribution of molluscs across a pneumatophore boundary in a small bay in northwestern Australia. Journal of Molluscan Studies 52, 83e90. Whitlatch, R.B., Hines, A.H., Thrush, S.F., Hewitt, J.E., Cummings, V., 1997. Benthic faunal responses to variations in patch density and patch size of a suspension-feeding bivalve. Journal of Experimental Marine Biology and Ecology 216, 171e189. Williams, B.G., Naylor, E., Chatterton, T.D., 1985. The activity patterns of New Zealand mud crabs under field and laboratory conditions. Journal of Experimental Marine Biology and Ecology 89, 269e282. Woodroffe, C.D., 1982. Litter productions and decomposition in the New Zealand mangrove, Avicennia marina var. resinifera. New Zealand Journal of Marine and Freshwater Research 16, 179e188. Woodroffe, C.D., 1985. Studies of a mangrove basin, Tuff Crater, New Zealand: I. Mangrove biomass and production of detritus. Estuarine, Coastal and Shelf Science 20, 265e280. Young, B.M., Harvey, L.E., 1996. A spatial analysis of the relationship between mangrove (Avicennia marina var. australasica) physiognomy and sediment accretion in the Hauraki Plains, New Zealand. Estuarine, Coastal and Shelf Science 42, 231e246. Zhuang, S., Wang, 2004. The influence of body size, habitat and diet concentration on feeding of (Laternula marilina) Reeve. Aquaculture Research 35, 622e628.