High diversity of tropical intertidal zone sponges in temperature, salinity and current extremes
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Afr. J. Ecol. 1999, Volume 37, pages 424–434
High diversity of tropical intertidal zone sponges in
temperature, salinity and current extremes
DAVID K. A. BARNES
Department of Zoology & Animal Ecology, University College Cork, Cork, Ireland, and
Frontier, Society for Environmental Conservation and Exploration, 77 Leonard Street,
London, U.K.
Abstract
The wide intertidal zone of the Quirimba Archipelago (Mozambique, East Africa)
encompasses many different habitats, which all experience wide environmental
variation. Large daily fluctuations in temperature occur when standing water is
heated up at low tide to >10°C above ambient. Salinity may be high in the dry
season and periodically almost fresh in the wet season. Very high current velocities
(≈3 ms−1) may occur and the direction of water flow is often complex. Sponges
were a major component of the fauna (and dominate the sessile forms) in most of
the eight habitats studied: exposed reef, sheltered reef, sand-rock, cave, reef boulders,
boulders on sand, mangrove swamp and seagrass meadows. The highest number of
sponge species occurred in the two reef habitats: from mean values of between ≈2.5
and ≈0.5 species/m2 (upper and lower shore, respectively). The diversity of species
present yielded a high Shannon index value of H=2.95 for the total of 33 species.
A rank-abundance plot of the data showed a high level of equitability (J=0.84).
Community similarity measurement using Bray–Curtis index showed two clusters;
the exposed habitats of the reefs and sand-rock and the refugia of cave, reef and
sand boulders.
Key words: Africa, diversity, extreme environment, intertidal, sponge
Résumé
La large zone d’estran de l’Archipel de Quirimba, au Mozambique, Afrique de
l’Est, comprend de nombreux habitats différents qui connaissent tous d’importantes
variations environnementales. De grandes amplitudes quotidiennes de température
s’observent lorsque l’eau stagnante est réchauffée à marée basse jusqu’à atteindre
10° de plus que l’air ambiant. La salinité peut être élevée en saison sèche, et l’eau
est presque fraı̂che périodiquement, en saison des pluies. On peut observer une très
grande vitesse de courant (≈3m/s.), et la direction du flux d’eau peut être complexe.
Les éponges étaient un des composants principaux de la faune (elles dominent les
formes sessiles) dans la plupart des huit habitats étudiés: récif exposé, récif abrité,
rochers sableux, cavernes, roches de récifs, roches de récifs sur sable, marais de
mangroves et prairies d’algues. On trouvait le plus grands nombres d’espèces
Correspondence: David K. A. Barnes. Fax: +353 21 274097, E-mail: dkab@ucc.ie
1999 East African Wild Life Society.East African intertidal zone sponge ecology 425 d’éponges dans les deux habitats de récifs: des valeurs moyennes d’environ 2,5 et 0,5 espèces/m2 (pour les limites supérieure et inférieure respectivement). La diversité des espèces présentes justifiait une valeur élevée de l’indice de Shannon (H=2,95) pour le total des 33 espèces. Un classement des données par ordre d’abondance montrait un haut degré (J=0,84). La mesure de la similarité des communautés au moyen de l’indice de Bray-Curtis montrait deux groupements: d’une part, les habitats exposés des récifs et les roches sableuses et d’autre part, les refuges des cavernes, des récifs et des roches de récifs sur le sable. Introduction Sponges of the class Demospongiae have colonized, and are often abundant, in virtually every major aquatic habitat known. They span almost the entire bathymetric, substratal, salinity and temperature ranges known in aquatic habitats (Bergquist, 1978). This ability not only to colonize but to thrive in a spectrum of habitats results partly from being (arguably) colonial (Larwood & Rosen, 1979) and clonal (Hughes, 1988). Coloniality may confer advantages in adaptive and ‘plastic’ morphology, maximum utilization of available space and in competition for existing space through indeterminate growth and survival of partial mortality. Suspension filtration, as a method of feeding, is also highly prevalent across habitats, and colonial forms have lack of size restriction and efficiency advantages in surface area of feeding apparatus to body volume compared to solitary forms. Perhaps more importantly though are a number of unique features of the phylum and the class Demospongiae in particular; structural simplicity, regenerative and reproductive capacity and close symbioses with micro-organisms. The Quirimba Archipelago in northern Mozambique is situated on a broad shelf and most of the islands have intertidal zones in excess of 500 m wide (tidal range 1–4 m). Around the periphery of these small islands a relatively wide range of intertidal habitats is encompassed. The wide intertidal zone of the Quirimba Ar- chipelago experiences large fluctuations in temperature, as the shallow pools and interstitial water may be heated up at low tide to >10°C above local sea temperature (pers. obs.). During this period in the dry season the salinity increases substantially. In the wet season, by contrast, river runoff may cause the intertidal zone water to be nearly fresh (M. Whittington, pers. comm.). The intensity of water flow varies daily with magnitude of tide and wind but can be complex in terms of direction and reach estimated velocities in excess of 3 ms−1 (Barnes & Whittington, 1999). Although the region is characterized by many physical extremes, the mobile epibenthos may be extremely diverse (e.g. hermit crabs, Barnes, 1997). Mobile inhabitants largely avoid these extremes by retreating to refugia (e.g. vertical migration in hermit crabs, Barnes, 1997). For sessile inhabitants, however, these extremities cannot be escaped and thus pose more of a survival problem. This study asks: (1) What is the contribution of sponges to the intertidal zone communities of the Quirimba Archipelago and how does this change with habitat and shore height? (2) How are the species and morphology types distributed, is there clear zonation? (3) Are there similarities between the communities of different habitats of similar exposure? (4) Are there special structural features of intertidal sponge species that can be interpreted as minimizing adverse environmental conditions? East African Wild Life Society, Afr. J. Ecol., 37, 424–434
426 David K. A. Barnes
Study site and methods
Eight intertidal zone habitat types were surveyed in the Quirimba Archipelago,
Mozambique: exposed coral reef, sheltered coral reef, sand rubble, cave, reef shore
boulders, sandy shore boulders, mangrove swamp and seagrass meadows. The coral
reef habitats studied are amongst some of the least anthropogenically disturbed in
East Africa (Barnes et al., 1998) and are highly speciose. The sand rubble/rock shore
is mainly characterized by highly abundant gastropod molluscs and hermit crabs
(Barnes, 1997). The mangrove swamps are characterized by the tree species Avicennia
marina, Ceriops tagal, Rhizophora mucronata and Brugieria gymnorhiza, and the
fauna is dominated by gastropod molluscs and decapod crustaceans. The seagrass
meadows are characterized by the angiosperms Halodule sp. and Cymodocea sp. The
associated fauna is ophiuroid and bivalve mollusc dominated.
In each area, the macro-epifauna in five randomly placed, 1-m2 quadrats were
examined every 10 m along transects from Extreme High Water Spring (EHWS) to
Extreme Low Water Spring (ELWS) tide levels. The intertidal shelf width at Quirimba
Island permitted a minimum of 175 and a maximum of 290 quadrats within-habitat
sample size. In each quadrat all macro-epifauna were identified to the lowest possible
taxonomic level, counted and in the case of sessile forms percentage coverage was
additionally recorded. The data were then subdivided into seven tidal levels based
on the period of emersion within a tidal cycle. From the data collected the mean
number of sponge species, mean sponge proportion of macro-fauna and mean sponge
proportion of sessile fauna or space occupation (all per m2) were calculated. The
sponge community diversity was investigated using standard methodology (Gray,
1987): diversity was calculated using the Shannon diversity index and the equitability
calculated using the Shannon equitability index. A rank-abundance plot was con-
structed of the sponge community to analyse shape relative to other communities.
The sponge community composition was analysed and compared between habitats
using the Bray–Curtis index of similarity.
Results
Sponge importance in extreme intertidal zone communities
A total of 33 species of sponge was recorded from the intertidal study zones in the
Quirimba Archipelago. The identity of the sponges found, and their location by
habitat and shore height, is shown in Table 1. There was distinct zonation of species
with shore height, with a number of species restricted to either the lower, mid- or
upper shore. No species was present at all shore heights, although two were present
at all but the highest and one present at all but the lowest. No sponges in this study
were recorded with any epibionts; all other shore fauna observed had epibionts on
at least some individuals.
The most common morphology of sponges in all habitats was encrusting, but
tubular forms were present in all but the mangrove habitat (Table 2). Encrusting
and tubular species were generally restricted to the lower shore or the shaded
habitats. More than 85% of individuals were encrusting in each of the four shaded
habitats (reef boulders, sand boulders, cave and mangrove). With the exception of
reef boulders, only one other sponge morphology was represented in the shaded
habitats. In the non-shaded habitats, by contrast, the proportion of encrusting species
East African Wild Life Society, Afr. J. Ecol., 37, 424–434East African intertidal zone sponge ecology 427
Table 1. Sponges occurring in the intertidal zone study sites in the Quirimba Archipelago
listed by genus/species. The habitats are Seagrass (Sg), Sand (S), Reef (R), Mangrove (M)
and Boulders (B) and Cave (C)
Period of emersion (hours in one tidal cycle)
Sponge taxa 0–1 2–3 4–5 6–7 8–9 10–11
C. Calcarea
Clathrina sp. Sg Sg Sg B
C. Demospongiae
Aaptos sp. Sg Sg S S
Aplysina sp. S S
Axinyssa sp. R R R
Biemma sp. MS MS
Callyspongia sp. R R
Carteriospongia foliascens R R
Cinachyrella voeltzkowii S S S S
Ciocalypta sp.1 S S S
Ciocalypta sp.2 SR SR
Dysidea sp. RB RB RB B B
Gelliodes sp. R R
Geodia crustosa CB CB C
Haliclona sp.1 M Sg M Sg
Haliclona sp.2 CB CB C
Haliclona sp.3 RB RB B
Iotrochota sp. R
Jaspis sp. R R
Lendenfeldia dendyi R R
Lissodendoryx sp. CB CB CB
Placospongia melobesioides R RB RB
Plakortis sp. S S SR SR S
Pseudosuberites andrewsi RB RB RBC BC BC
Sigmadocia sp. B B C
Spheciospongia florida S S SR SR
Spongia sp. Sg Sg
Tedania anhalens B CB CB C
Tedania digitata M M M M
Thalysias sp. Sg Sg
Xestospongia sp. R
Unidentified sp. R R
Unidentified sp. R R RC
Table 2. Proportions (%) of the sponge community in various morphological types for the
habitats sampled in the Quirimba Archipelago
Habitat Encrusting Spherical Leaved Buried Tubular Lobate Other
Exposed reef 32.6 3.3 31.5 1.1 6.5 21.7 3.3
Sheltered reef 37.2 5.8 18.6 3.5 8.1 24.4 2.3
Sand-rock 43.1 19 8.6 6.9 22.4
Seagrass 65.1 20.9 14
Reef boulders 91.5 2.1 6.4
Sand boulders 86.9 13.1
Mangrove 91.9 8.1
Cave 96.8 3.2
East African Wild Life Society, Afr. J. Ecol., 37, 424–434428 David K. A. Barnes
was < 66% and between three and seven morphologies were represented. Lobate
forms (e.g. Axinyssa sp.) were abundant in non-shaded habitats and absent from
those which were shaded. The two reef habitats had the greatest variety of morphology
and were the only habitats in which leaved forms occurred. Spherical forms were
only common in the sand-rock habitat, which was the most prone to extreme
temperatures and desiccation during the study period.
The mean number of sponge species (m−2) found in the study habitats was highest
on the lower shore, but in four habitats sponges occurred high on the upper shore
with 10.5 h immersion per tidal cycle. The highest level occurred in the three shaded
hard substratum habitats: reef shore boulders, sandy shore boulders and caves. Here,
sponge diversity decreased from ≈2 species m−2 at ELWS to ≈0.6 species m−2 at
9 h emersion per tide. The total number of sponge species, however, was greatest
on the open reef shores (9 at ELWS decreasing to 5 at 9 h emersion) up to upper-
mid-shore. From this level to 10.5 h emersion, the cave habitats had the highest
total number of species. The mangrove swamp was the poorest with just three species
recorded. There was no decline of sponge species with shore height on the sand-
rock habitat (except at the high water mark).
The proportion of fauna (by individuals) represented by sponges generally de-
creased with the period of emersion, but still represented up to 20% of the total
fauna and 50% of the sessile fauna on the upper shore. As with diversity, the values
were highest on reef and sandy shore boulders and lowest in the mangrove and
seagrass habitats (≈2%). Of the sessile communities, sponges (and polychaetes) were
the most important taxa, and in particular they dominated the sand-rock and boulder
environments (Fig. 1). Whilst sponges represented > 25% of the sessile fauna (by
individuals) in the seagrass meadows, they represented just 2.5% of the total fauna
there.
Sponge diversity was measured with the Shannon diversity index using base e,
yielding a value of H=2.95 for the total of 33 species. The community equitability
measured using the Shannon equitability index (again using base e) yielded a value
of J=0.84. The rank-abundance plot constructed (Fig. 2) exhibits the ‘broken stick’
form indicative of a high level of equitability, similar to that found in the most
mature terrestrial habitats studied by Bazzaz (1975).
Sponge community similarity and individual adaptations
The sponge communities of the exposed and sheltered reefs were similar in com-
position, as were those in the cave and reef boulder environments (Fig. 3). The
sponge communities of refugial environments also formed another similar cluster,
with that on boulders on sand being < 0.4, similar to either those on reef boulders
or in caves. The mangrove and seagrass communities differed considerably from all
others and each other. Intertidal sponge communities in the Quirimba Archipelago
could therefore be described as broadly belonging to one of four groupings: exposed,
refugial, mangrove and seagrass.
Sponges occurring in the shaded or ‘refugial’ environments were principally
encrusting forms (e.g. Haliclona sp.) and showed little obvious macro-morphic
adaptations to reduce the effects of thermal, desiccation and salinity extremes. Those
in the non-shaded hard substrata environments, however, showed a number of
adaptations to minimize the influence of environmental extremes. Many species had
East African Wild Life Society, Afr. J. Ecol., 37, 424–434East African intertidal zone sponge ecology 429 Fig. 1. Proportion of sessile fauna represented by sponges with period of emersion in hours (0=Extreme Low Water Neap tide level, 12=Extreme High Water Neap tide level) in the Quirimba Archipelago. Data are presented on three different scales for ease of interpretation. Fig. 2. Rank abundance for Quirimba Island sponge community. Note the log-scale for proportional abundance on the y-axis. a low surface area to volume ratio (e.g. Spirastrella sp.) and were peripherally toughened (e.g. Cinachyrella voeltzkowii) or pocketed to trap water (e.g. Lendenfeldia dendyi). Adaptations of sponges in non-shaded soft substrata included partial burial East African Wild Life Society, Afr. J. Ecol., 37, 424–434
430 David K. A. Barnes
Fig. 3. Bray–Curtis similarity index dendrogram for the study sponge communities of the Quirimba
Archipelago. Degree of similarity is shown on x-axis. Dotted lines have been added to aid interpretation
of clustering.
(e.g. Ciocalypta sp.), had occasional ‘keyholes’ (e.g. Spheciospongia sp.) or were
highly porous, so trapping high volumes of water (Clathrina sp.). In addition, some
sponge species, which also occurred in the subtidal zone, showed a great deal of
bathymetric morphological plasticity. The only sponge species present in the non-
shaded habitats above the point of 7 h emersion per tidal cycle were those with
one or more of the above adaptations. The spherical and toughened Cinachyrella
voeltzkowii was the only sponge species present in the non-shaded habitats above
the point of 9 h emersion per tidal cycle. Encrusting species, present in both shaded
and non-shaded habitats, occurred higher up the shore in the shaded habitats.
Similarly, within the shaded habitats, encrusting species, present on boulders and in
caves, occurred higher up the shore in the more shaded caves.
Discussion
The ubiquitous and abundant nature of sponges has been linked to a number of
aspects of their biology and ecology. Firstly, low tissue to skeletal matrix values and
tissue toughness have been argued as a key factor in maintaining low predation
levels (Barthel, 1995; Chanas & Pawlik, 1996). Secondly, the toxicity of many sponge
genera may be important in deterring predation (Pawlik et al., 1995). Toxicity may
also reduce competitor reproductive condition (Stocker & Underwood, 1991) or
recruitment (Davis et al., 1991). Thirdly, organizational (Gaino et al., 1995) and
morphological (Hartman, 1957) plasticity is undoubtedly important, particularly in
the intertidal zone. Fourthly, both asexual reproductive and regenerative capacity
allows the potential of both rapid colonization and damage recovery (Wulff, 1991).
Fifthly, close associations with bacterial symbionts has also been considered as
fundamental to sponge efficiency (Vacelet & Donaday, 1977).
The intertidal shelf regions in the Quirimba Archipelago are characterized by
environmental extremes in temperature, salinity and current velocity. To a lesser
extent they can also experience instability and turbidity from moving sediments or
storm disturbance. Sponges with low surface area to volume ratio and thickened
East African Wild Life Society, Afr. J. Ecol., 37, 424–434East African intertidal zone sponge ecology 431 periphery, or which are partially buried, are abundant at shore heights in the Quirimba Archipelago with more than 8 h immersion in a 12-h period. Close to thermal extremes, sponges may grow very slowly (Fowler & Laffoley, 1993), although some Antarctic species are known to grow comparatively fast (Dayton, 1989). Experimental studies on Suberites domuncula have shown up to a 50% reduction in the activity of certain enzymes when exposed to a 10°C rise in temperature for 20 min (Bachinski et al., 1997). Reports of the trends of persistence and invasion by sponges in habitats exposed to regular or irregular disturbance are, however, mixed in the literature. Large erect sponges may have reduced biomass and abundance following disturbance, whilst smaller sponges under similar conditions are invasional (Wulff, 1995). Fabricius (1996), in contrast, found no increased cover by sponges after Acanthaster planci outbreaks reduced coral cover on the Great Barrier Reef. The sessile intertidal zone communities in the Quirimba Archipelago are com- paratively depauperate, but sponges were common and represented by 33 species. They were also extremely ubiquitous, as all intertidal habitats in the present study were colonized by sponges to some extent. The area in which sponges achieved greatest importance was in the cryptic communities (boulders and caves), where they dominated the communities. This is at least partly related to light levels, as littoral sponge diversity has been described as negatively correlated to irradiance levels (Uriz et al., 1992). Although high abundance, specific and morphological diversity has been recorded from sublittoral polar waters, sponges are rare in the immediate subtidal zone and unrecorded from the intertidal zone (Dayton, 1989). In temperate waters, sponges are frequently recorded in the intertidal zone, but their diversity is low even at localities with high sublittoral numbers, such as Lough Hyne in Ireland (Picton, 1991). In tropical intertidal zones, by contrast, sponges are typically more abundant, specifically and morphologically diverse (Bergquist, 1978). However, the intertidal zone diversity reported in this study is the highest known (within a study area of comparable size) to the author. The range of sponge morphological form in the Quirimba I intertidal zone was almost as high as that of the adjacent subtidal reefs (D. K. A. Barnes, unpubl. obs.). Table 3 shows shore and shallow water trends within the sponges. Cnidarians show similar patterns of abundance and diversity with latitude; very low in polar waters, poor diversity and morphological variation in temperate waters and high diversity and morphological variation in tropical reefs. Unlike sponges, however, they are generally restricted to the lower shore. Other colonial taxa show quite different patterns with latitude; bryozoans and ascidians probably reach greatest abundance and diversity on temperate shores but have little morphological variability. Phoronans, entoprocts and pterobranch hemichordates are rarely recorded from intertidal localities at any latitude. Thus, sponges of intertidal tropical waters illustrate the greatest morphological variation of any littoral colonial invertebrates at any latitude. The taxon is also the least restricted to lower shore of any littoral colonial invertebrates at any latitude. The structure of sponge communities were of four broad groupings: exposed, refugial, mangrove and seagrass meadows. The similarity and high numbers of species and morphologies occurring in the exposed habitats is probably in part due to habitat complexity, particularly in the case of the reefs. The surfaces of boulders East African Wild Life Society, Afr. J. Ecol., 37, 424–434
432
David K. A. Barnes
Table 3. Environment parameters and influences/probable influences on sponge communities. All influences in table (e.g. abundance) are
increases unless otherwise stated
Parameter Intertidal zone Subtidal zone
⇓ Latitude Abundance High abundance, specific & morphological
Specific diversity diversity in polar & tropical regions
Morphological diversity
Shore height tolerance
⇑ Substratum stability Abundance Abundance
Specific diversity Specific diversity
Morphological diversity Morphological diversity
East African Wild Life Society, Afr. J. Ecol., 37, 424–434
⇑ Substratum complexity Specific diversity Specific diversity
Morphological diversity Morphological diversity
⇑ Substratum secondary space availability Abundance Abundance
Specific diversity Specific diversity
⇑ Immersion period (depth) Abundance Abundance
Specific diversity Specific diversity
Morphological diversity
⇑ Shade (caves, crevices) Abundance Abundance
Specific diversity Specific diversity
⇑ Water flow Unknown Abundance
Specific diversity
⇑ Organic input Unknown Probably
Abundance
Specific diversityEast African intertidal zone sponge ecology 433
and caves are fairly uniform by comparison; however, the shaded element to these
habitats would also reduce the requirement for structural adaptations to reduce
desiccation. Zonation of sponges by species and by morphology was distinct. That
sponges are so prevalent in these habitats may actually be a result of the variety of
environmental extremes which they seem to be able to withstand, in the Quirimba
Archipelago, to a greater extent than any other sessile taxon.
The great majority of sponges occurring in the cryptic or refugial habitats of caves
and undersurfaces of boulders in the present study were of encrusting morphology
(e.g. Haliclona sp.). Under-surfaces of boulders and caves give some protection from
temperature, current extremes and through trapping pools help reduce evaporation,
so reducing desiccation and salinity changes. The actual environmental extremes
experienced by intertidal sponges in such habitats is therefore minimized. Erect
lobate forms, such as Thalysias sp. which occurred in seagrass meadows, were
restricted to pools so were only ever partially immersed. However, even in exposed
environments such as sand-rock sponges dominated the sessile fauna. Here a variety
of structural adaptations helped to reduce environmental extremes. These included
either filling cavities (in rock), growing into and entwining with other sponges and
near spherical shape, all resulting in a low surface area to volume ratio (e.g. Plakortis
sp.). Damage resistance and desiccation reduction must also be improved by a
toughened outer layer such as possessed by Cinachyrella voeltzkowii. The sole but
abundant presence of C. voeltzkowii on the upper non-shaded shore suggests that
this might ultimately be the most effective strategy.
Acknowledgements
The author wishes to thank all the members of the Darwin/Frontier Mozambique
Marine Research Programme. This is a collaborative venture between the Society
for Environmental Exploration (SEE) in the U.K. and the Ministépara a Coordenação
de Acção Ambiental (MICOA) in Mozambique and is part funded by the Darwin
Initiative for the Survival of Species (Department of the Environment, U.K.).
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