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ATOLL RESEARCH BULLETIN
NO. 515
EXTRAORDINARY MOUND-BUILDING FORMS OF AVRAINVILLEA
(BRYOPSIDALES, CHLOROPHYTA): THEIR EXPERIMENTAL TAXONOMY,
COMPARATIVE FUNCTIONAL MORPHOLOGY AND ECOLOGICAL STRATEGIES
BY
MARK M. LITTLER, DIANE S. LITTLER, AND BARRETT L. BROOKS
ISSUED BY
NATIONAL MUSEUM OF NATURAL HISTORY
SMITHSONIAN INSTITUTION
WASHINGTON, D.C., U.S.A.
SEPT EMBER 2004
Figure 1. The Central Province of the Belize Barrier Reef showing the study sites on Twin Cays and
Curlew Cay.
EXTRAORDINARY MOUND-BUILDING FORMS OF AVRAINVILLEA
(BRYOPSIDALES, CHLOROPHYTA): THEIR EXPERIMENTAL TAXONOMY,
COMPARATIVE FUNCTIONAL MORPHOLOGY AND ECOLOGICAL
STRATEGIES
BY
MARK M. LITTLER, DIANE S. LITTLER, AND BARRETT L. BROOKS
ABSTRACT
The discovery of astounding mound-building colonial forms of Avrainvillea (to 30 m
diam.) dominating the standing stocks and productivity of submerged habitats within Belizean
mangrove island interior creeks, ponds and lakes catalyzed this study. The mound formers (f.
laxa and f. olivacea), which we initially hypothesized to be undescribed species, presented
unresolved taxonomic questions. A common-garden reciprocal-transplant approach showed
that following one year all experimental transplants had acquired the morphological features
consistent with the taxa characteristic of the new habitats, thereby falsifying the hypothesis that
the mound formers were distinct species.
After one year, 2- to 3-blade clumps transplanted from Twin Cays to Curlew Cay had
developed rudimentary stages of massive holdfast with the adherent sand grains characteristic of
f. longicaulis and f. asarifolia. Conversely, all of the morphs with normally massive holdfasts
that were transplanted to the mangrove pools at Grouper Gardens showed degeneration of the
columnar holdfasts, with only remnant rhizoids containing clumped sand grains present at the
end of one year. Concurrently, all of these plants developed new assimilators/stipes
characteristic of the colonial morphs (f. laxa and f. olivacea). Both sets of controls and
transplant controls were 100% uniform in retaining morphs consistent with their original habitats.
The large colonial mangrove morphs (i.e., f. laxa and f. olivacea) were not resistant to
even the moderate current levels (3.6±0.5 cm per sec) encountered in the back-reef lagoon
habitats of the deeply anchored morphs (i.e., f. longicaulis and f. asarifolia).
In support of the perennation hypothesis, only the experimentally amputated Curlew
Cay morphs (both f. longicaulis and f. asarifolia) showed significantly more proliferations
(100 %) than either the amputated Twin Cays morphs (both f. laxa and f. olivacea) or the
uncut Curlew and Twin Cays control morphs. The stipes and blades of the open-water morphs
(Avrainvillea longicaulis f. longicaulis and A. asarifolia f. asarifolia) serve as expendable
assimilators with a major function of building a massive perennating/storage organ, the columnar
holdfast, which comprises the bulk of the plant. Physical disturbances (such as storms and
herbivory), as well as physiological stresses (such as epiphyte loading), can cause
disproportionate losses of the relatively delicate expendable assimilators which are replaced
subsequently by perennation from the long-lived subterranean holdfast during more favorable
conditions.
__________________
Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington DC
20560-0166
2
INTRODUCTION
Overall, the ecology of siphonaceous green algae (Bryopsidales) is not well known even
though members of this group occur abundantly in virtually all tropical open-water reef and
lagoon habitats. The discovery of three incredible mound-building colonial forms [=morphs or
forma (f.)] of Avrainvillea, dominating the standing stocks and productivity of submerged
habitats within Belizean mangrove island interior creeks, ponds and lakes, literally demanded
this study. These persistent mound-formers are restricted to shallow (<3 m), calm, peat-
bottom, high-nutrient waters in the protected interiors of mangrove islands.
Lagoons of the Belize Barrier Reef Central Province, such as those westward of Carrie
Bow Cay and Curlew Cay (Fig. 1), are the most extensive of the entire reef tract including
diverse and abundant populations of sand-dwelling macroalgae and seagrasses. These back-
reef environs comprise a well-developed lagoonal system remote from major human pollutants.
Organic detritus rarely accumulates on coral-dominated reefs because of intense herbivory and
export processes. However, the characteristic nutrient limitation patterns typically observed in
tropical reef systems are not applicable to the detritus-rich mangrove-peat systems of Twin
Cays (Lapointe et al., 1987), which are characterized by elevated nutrient availability.
In general, mangrove ecosystems are well-known for their high levels of marine
compost (Fell et al., 1980; Newell et al., 1984) that release relatively high concentrations of
dissolved inorganic nitrogen and phosphates (Snedaker and Brown, 1981) into the adjacent
water column. Considering that nutrient uptake kinetics in macroalgae are highly concentration
dependent, mangrove macroalgae have been shown (Lapointe et al., 1987) to be far less
nutrient-limited compared to macroalgae on coral reefs, based on seawater and tissue analyses
as well as nutrient limitation/bioassays performed at the identical sites investigated here (i.e.,
Curlew Cay and Twin Cays, Fig. 1). Also, the geology, natural history and biology of these
systems are comparatively well-known as a result of over three decades of multidisciplinary
investigations (see Rützler and Macintyre 1982, Rützler and Macintyre this volume).
The rhizomatous (“rooted”) Bryopsidales are considered to be important stabilizers of
both organic and carbonate sediments. It also has been documented (Williams and Fisher,
1985; Littler et al., 1988; Littler and Littler, 1990) that the rhizoidal sand-dwelling forms of the
open lagoon play a significant role in cycling nutrients from sediment pore waters. Rhizophytes
such as Avrainvillea, Udotea, Halimeda, Penicillus, Rhipocephalus, Cladocephalus and
Caulerpa (Chlorophyta, Bryopsidales) are among the predominant contributors to macroalgal
cover and primary productivity within the vast seagrass meadows throughout the tropical
western Atlantic. Such “rooted” plants, by tapping into the nutrient-rich interstitial pore waters
(Littler and Littler, 1988), can avoid many of the nutrient-limitation problems experienced by
their rock-dwelling counterparts.
While seagrasses and diverse macroalgal phyla are abundant on the outer perimeters of
Twin Cays (Fig. 2, Littler et al., 1985), it is the siphonaceous Chlorophyta that dominate the
standing stocks and productivity of submerged interior habitats within the mangrove island
proper. In particular, the genus Avrainvillea is conspicuous among the predominant
contributors to biomass and primary productivity within the vast array of creeks, ponds, lakes
and borders of Twin Cays. Some members of the siphonaceous green algae characteristic of
Twin Cays contain unique and interesting secondary chemical compounds (Sun et al., 1983;
3
Figure 2. Oblique aerial view of Twin Cays (looking east) showing the many hidden lakes and ponds.
The Grouper Gardens study site is labeled on the upper right.
Figure 3. Colonial sea anemones using Avrainvillea blades as an attachment substrate.
4
Figure 4. The cryptic crab
Thersandrus compressus (arrow) is
a specialist feeder on Avrainvillea
that has a negative impact (Hay et
al., 1990; Littler and Littler, 1999).
Hay and Fenical, 1988) and highly specialized interactions between the larger forms (e.g.,
Udotea, Avrainvillea, Caulerpa, Penicillus) and such herbivorous invertebrates as crabs and
molluscs have been observed (Hay et al., 1990; Littler and Littler, 1999). Avrainvillea
provides microhabitats (Fig. 3), as well as food and shelter (Fig. 4), for many meso- and micro-
invertebrates. These one-sided associations have proven (Hay et al., 1990) to be primarily
beneficial to the invertebrates and detrimental to the algal host.
The mucilage-free spongy textures of Avrainvillea would seem to make them
susceptible to epiphytic plant/animal loading. However, we showed in an earlier study (Fig. 5,
Littler and Littler, 1999) that the solitary lagoon morphs are able to rapidly produce new fronds
by cytoplasmic streaming and translocation through their siphons, a process that is not impaired
by cross walls (as is the case of cellular plants). This represents a unique antifouling mechanism
(Littler and Littler, 1999) whereby old assimilators and their inhibitory epiphytes can be shed by
“blade abandonment/proliferation” at relatively low cost to the plant.
5
A major obstacle to understanding the ecological role of siphonaceous algae at Twin
Cays has been the high biodiversity of the taxonomically problematical genera named above.
Six distinct species of Avrainvillea co-occur in the creeks, ponds and lakes of Twin Cays
(Figs. 6, 7). Using treatments prior to the beginning of this investigation (Taylor, 1960; Norris
and Bucher, 1982), it would have been possible to discern only a small fraction of the taxa that
are actually present. As one example, Avrainvillea longicaulis f. longicaulis (Fig. 6) and the
similar appearing A. mazei (Fig. 7) co-occur at Twin Cays as well as throughout lagoonal grass
bed habitats and require precise discrimination (see misidentification of A. mazei, as A.
longicaulis, on page 225 of Humann and DeLoach, 2002). In fact, there had been no serious
systematic work on the group since the turn-of-the-century (Gepp and Gepp, 1911) with the
Figure 5. The paddle-like blades of the lagoon forms of Avrainvillea (A) can rapidly translocate
protoplasm to proliferate new epiphyte-free blades (B-natural epiphytes, C-mesh bag).
A
C
B
6
Figure 6. The three species shown here (Avrainvillea nigricans f. spongiosa, A. asarifolia f. olivacea
and A. longicaulis f. laxa) create large mound-like colonies in mangrove lakes and ponds.
exceptions of herbarium-based treatments of Halimeda (Hillis-Colinvaux, 1980) and Pacific
Avrainvillea (Olsen-Stojkovich, 1985). The systematic monograph on tropical western
Atlantic Avrainvillea (Littler and Littler, 1992), as well as the floristic field guide for the nearby
Pelican Cays (Littler and Littler, 1997), alleviated the major taxonomic stumbling blocks and
enabled this study.
Experimental Organisms
As mentioned, the siphonaceous green algal genus Avrainvillea often dominates the
standing stocks and productivity of submerged habitats within mangrove island creeks, ponds
and lakes as well as occurring abundantly throughout virtually all calm-water reef systems.
7
Figure 7. The three species shown
here occur as individuals at Twin Cays
but do not form colonial mounds.
Although sporogenic reproduction has never been reported for Belizean Avrainvillea, rare
club-shaped release structures produced at the tips of individual blade siphons have been
observed elsewhere (Littler and Littler, 1992). Unlike other Bryopsidales, species of
Avrainvillea are long-lived (see Littler and Littler, 1992) and do not undergo holocarpy [i.e.,
mass synchronous sporogenesis (Clifton, 1997) followed by death and disintegration of the
entire thallus].
The experimental macroalgae Avrainvillea longicaulis f. longicaulis, A. longicaulis f.
laxa (Fig. 8), A. asarifolia f. asarifolia and A. asarifolia f. olivacea (Fig. 9) are particularly
abundant but mostly unstudied in the Belize Barrier Reef lagoon and mangrove islands. The
paddle-shaped blades (=flabella, caps or assimilators) of Avrainvillea number from one to
many and are broadly oval (to 24 cm high, to 29 cm wide) with truncated lower margins. They
are thick (> 4 mm) and spongy (lacking a mucilaginous coating) with cylindrical or flattened
stipes (to 12 cm long, 13 mm diam.). The blades, stipes and holdfasts are composed of
dichotomously branched interconnected siphons entirely lacking cross walls. The thalli of A.
8
Figure 8. The two dramatically different morphological forms (morphs) of Avrainvillea longicaulis
(f. longicaulis & f. laxa). However, note the anatomical (siphons) similarities.
Figure 9. The two dramatically different morphological forms of Avrainvillea asarifolia (f. asarifolia
& f. olivacea). However, note the anatomical (siphons) similarities.
9
Figure 10. The two dramatically different morphological forms of Avrainvillea nigricans (f. nigricans
& f. spongiosa). However, note the anatomical (siphons) similarities.
longicaulis f. longicaulis, A. asarifolia f. asarifolia and A. nigricans f. nigricans (Figs.
8, 9, 10) are typically anchored by a massive, perennating, bulbous, rhizoidal holdfast (Fig.
11) in open sandy or seagrass areas of shallow (to 30 m) pristine waters.
As emphasized above, the discovery of incredible mound-building colonial morphs of
Avrainvillea [A. longicaulis f. laxa (Fig. 8), A. asarifolia f. olivacea (Fig. 9) and A. nigricans
f. spongiosa (Fig. 10)] catalyzed this study. These three colossal mound-formers are restricted
to shallow (<3 m), placid, peat-bottom, high-nutrient waters in the protected interiors of
mangrove islands.
HYPOTHESES TESTED
Coloniality Hypothesis
To reiterate, Avrainvillea longicaulis f. longicaulis and A. asarifolia f.
asarifolia (Figs. 8, 9) are solitary in open lagoonal sandy environments with consistent
wave action but can form extraordinary decades-old colonial (possibly clonal?) mounds
(Fig. 12). The taxa, described (Littler and Littler, 1992) as A. longicaulis f. laxa (Fig.
8) and A. asarifolia f. olivacea (Fig. 9), are persistent in peaty, highly eutrophic, placid,
interior mangrove habitats. The f. laxa and f. olivacea morphs hypothetically (i.e.,
10
Figure 12. Portion of a colossal colonial mound
of Avrainvillea longicaulis f. laxa supporting
diverse epiphytes at Twin Cays.
Figure 11. The massive perrenating, bulbous,
rhizoidal holdfast of Avrainvillea longicaulis f.
longicaulis characteristic of open sandy lagoonal
areas.
“coloniality hypothesis”) are uniquely adapted to utilizing flabellar stipes as shallow
subterranean rhizomes that spread laterally to produce enormous (several meters-thick, to 30
m diameter, Fig. 12) mound-like colonies that overgrow rich organic peat bottoms. Massive
columnar rhizoidal holdfasts, such as those found in the f. longicaulis (Fig. 11) and f.
asarifolia (Fig. 9) morphs, hypothetically would be superfluous under placid enriched water-
column nutrient conditions as well as incapable of surviving the deeper anoxic conditions of
the composting peat deposits. Conversely, open-water wave surge and current drag on the
huge colonial morphs (lacking a strong anchoring rhizoidal holdfast that could augment the
low nutrient conditions in open lagoonal waters) should result in uprooting, wave-shearing
damage and general attrition.
Perennation Hypothesis
In the open-water morphs of Avrainvillea longicaulis f. longicaulis and A. asarifolia
f. asarifolia (Littler and Littler, 1992), we had observed what appeared to be perennation;
where the remains of lost blades were indicated by breakage points and scars with newly
forming flabella arising from either the former stipes or columnar holdfasts. We postulated (i.e.,
“perennation hypothesis”) that the stipes and blades of Avrainvillea longicaulis f. longicaulis
and A. asarifolia f. asarifolia serve as expendable photosynthetic assimilators with a major
function of building a massive perennial storage organ, the columnar rhizoidal holdfast. This
structure (Fig. 11) can comprise up to 90% of the total thallus (Olsen-Stojkovich, 1985; Littler
and Littler, 1999). In other words, physical disturbances (such as storms and herbivory) as well
11
Figure 13. Conducting primary productivity
experiments on Avrainvillea longicaulis f. laxa at
Twin Cays using oxygen electrode methods (Littler
and Littler, 1987).
as physiological stresses (such as epiphyte loading) should result in disproportionate losses of
the relatively delicate above-ground assimilators, which can be replaced by perennation from
the massive subterranean holdfasts (Fig. 11) during more favorable conditions.
METHODS AND MATERIALS
Experimental Taxonomy
The critical initial phase of this research included completion of a systematic and
phylogenetic monograph of Caribbean Avrainvillea based on intensive and extensive
collections throughout Twin Cays and surrounding environments (Littler and Littler, 1992). As
emphasized, the discovery of astounding mound-building persistent colonial morphs of
Avrainvillea motivated this study. However, taxonomic issues still prevailed regarding these
mound formers, which were initially thought by us to be distinct species although the internal
anatomical data suggested (Littler and Littler, 1992) otherwise. The experimental “common
garden” reciprocal transplant approach used here (see below) provided quantitative resolution
of these issues.
Coloniality Hypothesis
We used a costs vs. benefits approach to test the coloniality hypothesis (N=10/
treatment). We posited that the two sets of remarkably different morphs (i.e., f. laxa vs. f.
longicaulis and f. olivacea vs. f. asarifolia) are adaptive for their respective habitats. We
attempted to experimentally induce colony formation in the f. longicaulis and f. asarifolia
morphs by burial of the flabellar stipes as well as by conducting reciprocal transplant
12
experiments with appropriate control (C= tagged only) and transplant controls for both morphs.
In each habitat (i.e., Curlew Cay and Twin Cays, Grouper Gardens, Figs. 1, 2), the transplant
controls (TC) were completely removed by careful digging and gently replanted in holes wedged
opened by titanium crowbars in the nearby general area. The experimental transplants (T) were
carefully removed, floated into a 100-liter cooler of seawater and transferred to the reciprocal
field sites where they were carefully replanted as above.
As described earlier, this “common garden” approach also led to an experimental
taxonomic analysis of whether or not the various morphs might represent distinct species. All
replicates were tagged by nearby surveyors’ flags. After one year of growth, the plants were
returned to the laboratory for final photography and morphometric documentation. If we could
(1) induce coloniality in the individuals of f. longicaulis and f. asarifolia (under the presence of
high nutrients and benign physical conditions) within calm interior mangrove ponds and (2) show
that large colonies of f. laxa and f. olivacea are susceptible to removal by natural levels of
current and wave surge, then the coloniality hypothesis would be deemed to be supported. A
further bonus in support of the hypothesis would be (3) any sign of long-term induction of
columnar holdfasts in the f. laxa and f. olivacea transplants moved from mangrove island pools
into open water habitats.
Perennation Hypothesis
In addition, we concurrently tested the perennation hypothesis as follows: (1) in experi-
mental lagoon thalli with blades physically amputated, proliferation of new blades should be
stimulated and (2) moderate losses of blades should not lead to high levels of mortality relative
to control plants not subjected to such mutilation. Twenty separate plants of Avrainvillea
longicaulis f. longicaulis and another 20 of A. asarifolia f. asarifolia were assessed in the
lagoon behind Curlew Cay. Both sets were divided into the following two replicate groups
(N=10) by double randomization to provide: controls (CO, to correct for natural changes and
possible stochastic events) and cut plants (C, to simulate natural physical damage). All were
marked by surveyors’ flags.
The same procedure was repeated at Grouper Gardens for Avrainvillea longicaulis f.
laxa and A. asarifolia f. olivacea (N=10/treatment). After one year, the controls (CO, which
had been left intact) and the amputated/cut plants (C, which were trimmed with scissors, leaving
the intact holdfast and 2-cm stipe lengths) were assessed for blade numbers and new
proliferations. Data analysis employed ANOVA and the Bonferroni Test for significant
differences.
Ecological Role
To assess the ecological importance of the Avrainvillea longicaulis f. laxa mounds,
quantitative transect surveys of biotic cover were conducted using the nondestructive
photogrammetric techniques developed by Littler and Littler (1985). This entailed video
transects at right angles to the substrata that were then scored in stop action on a high-resolution
video monitor. Cover was determined by recording the percentages of point intercepts from a
randomized array superimposed over the video images. Two randomly selected 0.25 m
sections at the edges of two separate mounds were harvested for biomass determinations.
13
These were cleaned of peat deposits and epiphytes, photographed and weighed wet. A set of
subsamples from these were rinsed in freshwater, weighed, dried and reweighed to determine
wet-to-dry weight relationships. Organic dry-weight (ODW) was determined by igniting the
dried samples in a muffle furnace to constant weight at 500º C.
Primary productivity measurements were made for the dominant Avrainvillea
longicaulis f. laxa using traditional light-dark bottle oxygen electrode techniques (Fig. 13).
This, and the transect data, were used to ascertain an average mound’s contribution to primary
production at Twin Cays. We measured photosynthetic rates of the assimilators during early
summer under ambient environmental conditions (30–31º C, 36 ppt salinity, 1500–2100 µmol
photons per m2 per sec) using the same methods detailed in Littler and Littler (1990). We
incubated healthy assimilators containing natural levels of epiphytes and replicate blades with the
epiphytes carefully removed by pinching (Fig. 13), as well as incubating the epiphytes separately
(N =6 for all treatments), to ascertain the primary productivity contributions of the epiphytes.
We chose photosynthesis as an indicator of physiological production since growth is relatively
intractable due to the continual translocation processes and the inaccessibility of the stipe/
holdfast system. Data analysis employed ANOVA and the Bonferroni Test for significant
differences.
RESULTS
Experimental Taxonomy
The mound formers (f. laxa and f. olivacea), which were initially hypothesized to be
putative species (Littler and Littler, 1992), presented unresolved taxonomic questions. The
common-garden reciprocal-transplant approach provided definitive resolution of these issues.
Following one year of transplantation, all experimental transplants had acquired the
morphological features consistent with the taxa characteristic of the new habitats (Fig. 14, 15,
16, 17), thereby falsifying the hypothesis that the mound formers were distinct species.
Coloniality Hypothesis
The large colonial mangrove morphs (i.e., f. laxa and f. olivacea) were not resistant to
even the moderate current levels (3.6±0.5 cm per sec) encountered in the back-reef lagoon
habitats of the deeply anchored morphs (i.e., f. longicaulis and f. asarifolia). When buried to
normal depths, the massive natural colonial morphs would pull free and begin to drift
downstream (Figs. 18, 21). However, the majority of the 2- to 3-blade clumps (Fig. 15), with
their stipes deeply buried in the sandy sediments, were able to survive and grow.
After one year, the surviving 2- to 3-blade clumps transplanted from Twin Cays to
Curlew Cay had developed rudimentary stages of the massive holdfast with the adherent sand
grains (Fig. 15) characteristic of f. longicaulis and f. asarifolia. Conversely, all of the surviving
morphs with normally massive holdfasts that were transplanted to the mangrove pools at
Grouper Gardens showed degeneration of the columnar holdfasts (Fig. 17), with only remnant
rhizoids containing clumped sand grains present at the end of one year. Concurrently, they had
developed new assimilators/stipes characteristic of the colonial morphs (f. laxa and f.
olivacea). Both sets of surviving controls and transplant controls were 100% uniform in
retaining morphs consistent with their original habitats.
14
Figure 14. Examples of Avrainvillea longicaulis f. laxa transplanted from twin Cays to Curlew Cay
after 12 months. Blades now are consistent with the f. longicaulis morph.
Figure 15. Examples of Avrainvillea longicaulis f. laxa transplanted from twin Cays to Curlew Cay
and harvested after 12 months. Holdfasts now are consistent with the f. longicaulis morph.
15
Figure 16. Examples of Avrainvillea longicaulis
f. longicaulis transplanted from Curlew Cay to
Twin Cays after 12 months. Blades (draped in
flocculent peat sediments) now are consistent with
the f. laxa morph.
Figure 17. Examples of Avrainvillea longicaulis f. longicaulis transplanted from
Curlew Cay to Twin Cays and harvested after 12 months. Pseudo-rhizomatous
holdfasts and stipes now are consistent with the f. laxa morph.
16
Figure 18. A – Two individuals of Avrainvillea asarifolia f. asarifolia from Curlew Cay. B – Colony
of f. olivacea from Twin Cays. When both forms were transplanted to the back-reef sandy habitat,
the f. olivacea colony was uprooted by current within hours, whereas the f. asarifolia thalli remained
indefinitely.
We also discovered unexpected evidence in further support of the coloniality
hypothesis in the case of Avrainvillea longicaulis f. laxa. We found that the colonial
morphology is uniquely reinforced by the intermingling of blade and stipe siphons at
areas of contact (Figs. 19, 25). Contact frequently occurs for prolonged periods in
such calm habitats, leading to abundant anastomosing points of fusion/adhesion.
17
Figure 19. Typical inter-thallus
fusions characteristic of the
colonial mound-forming species.
Perennation Hypothesis
In support of the hypothesis (Fig. 20), only the experimentally amputated Curlew Cay
morphs (both f. longicaulis and f. asarifolia) showed significantly more proliferations (100 %)
than either the experimentally amputated Twin Cays morphs (both f. laxa and f. olivacea) or
the uncut Curlew or Twin Cays control morphs. In particular, the amputated Curlew Cay
Avrainvillea longicaulis f. longicaulis showed 100 % new proliferations, a significant fivefold
increase relative to the Twin Cays f. laxa (20 %). The uncut controls from Curlew Cay f.
longicaulis showed significantly fewer (70 %) new proliferations, whereas the Twin Cays
experimental f. laxa plants also had significantly fewer (50 %) new proliferations.
In the case of Avrainvillea asarifolia f. asarifolia from Curlew Cay (Fig. 20), the
experimentally amputated plants also had 100 % new proliferations paralleling the results for A.
longicaulis f. longicaulis. The experimentally amputated f. olivacea also showed significantly
fewer proliferations comparable to those for f. laxa (only 20 % new proliferations, significantly
less at P < 0.05). The uncut control morphs of A. asarifolia from both Curlew Cay (f.
asarifolia) and Twin Cays (f. olivacea) produced comparably low results as well, with
significantly fewer (40 %) new proliferations (Fig. 20).
18
Figure 20. The percent of plants with new proliferations following mutilation (blade decapitation by
cutting) after 12 mos. The massive holdfast morphs f. longicaulis and f. asarifolia from Curlew Cay
showed significantly greater proliferation following cutting than the uncut treatments or the uncut
and cut colonial mangrove morphs, f. laxa and f. olivacea. (* indicates significant differences at
P<0.05)
Ecological Role
One of the smaller Avrainvillea longicaulis f. laxa colonies measuring 0.6 X 1.1 m in
diam. (Fig. 21) and hand-cleaned of debris and epiphytes (mostly unusual forms of Laurencia
intricata, Cladophoropsis membranacea and Polysiphonia flaccidissima, Fig. 22) weighed
19 kg. Similar weights were recorded for comparable colonies of A. asarifolia f. olivacea
(Fig. 18). Given that transect studies documented that both A. longicaulis f. laxa and A.
asarifolia f. olivacea form colonies in excess of 30 m diam. (Fig. 12), their contribution to
biomass in Twin Cays ponds is enormous.
Epiphyte-free Avrainvillea longicaulis f. laxa blades showed a net photosynthetic rate
of about two-and-a-half mg C fixed per gram of organic dry mass (ODM) per h, with a dark
respiration rate of about half a mg C consumed per g ODM per h (Fig. 23). Twenty newly
formed blades (mean area = 50 cm2) contained an average of 12 mg ODM per cm2 (28 % C),
which converts to about four mg C per cm2 of proliferating blade. Given the net photosynthetic
production determined above (with the normal inhibitory effects of natural levels of epiphytes)
and assuming that this rate could be sustained throughout a 10 h-day, with dark respiration at
half a mg C consumed per g ODM per h for 14 h (not including respiration of the pseudo-
19
Figure 21. This small colony of Avrainvillea longicaulis f. laxa from Twin Cays weighed 19 kilograms
(spun wet weight).
Figure 22. Twenty meter diameter colony of Avrainvillea asarifolia f. olivacea at Twin Cays showing
the extensive coverage of epiphytes (predominantly unusual forms of Laurencia intricata,
Cladophoropsis membranacea and Polysiphonia flaccidissima).
20
Figure 23. The net primary productivity (light histograms) and respiration (dark) of Avrainvillea
longicaulis f. laxa blades with natural epiphytes, epiphytes removed and epiphytes alone.
rhizomatous mass), we arrived at a net rate of about four mg C per g ODM per day. The wet
samples yielded an average dry weight (DW) of about 7% of the WW. When ignited to
constant ash weight at 500º C, the organic dry mass averaged 79 % of the DW. Mature
assimilators produced about two mg C per plant (single stipe with blade) per day. Based on
these calculations, the productivity of an average single mound of Avrainvillea at Twin Cays
would conservatively yield an astounding 4 kg of carbon fixed per day. The productivity of a
square meter of an average mound calculates at 6.2 g of C fixed per day.
DISCUSSION
Taxonomy
Experimental field approaches to macroalgal taxonomic questions are seldom utilized
even though the rapid growth of most seaweeds makes them amenable to manipulative
techniques. The “common garden” reciprocal transplant experiment provided definitive
resolution of the hypothesis that the mound formers (f. laxa and f. olivacea) were discrete
species. Following one year of transplantation, all experimental transplants had acquired
morphological features that were consistent with the morphs characteristic of their new habitats
(Fig. 24). This result, and the internal anatomical data (Littler and Littler, 1992), supports the
hypothesis that the mound forms are not distinct from the solitary forms (f. longicaulis and f.
asarifolia) and, therefore, falsifies the hypothesis that mound-forming colonial taxa are separate
species.
21
Figure 24. Side-by-side comparison
of 12-month experimental transplants
showing the acquisition of morpho-
logical characters that were consistent
with the forms characteristic of their
new habitats.
Avrainvillea transplanted from Twin Cays ponds to Curlew Cay
(Fig. 15).
Figure 25. Avrainvillea longicaulis f. laxa showing tangled jumble of stipes and blades forming
extensive mounds in Twin Cays ponds. Note the tangled fused pseudo-rhizomatous stipe structure
adaptive for the flocculent anoxic peat substrate.
Avrainvillea transplanted from Curlew Cay to Twin
Cays Ponds (Fig. 17).
22
Coloniality
This study suggests that the ecological attributes of mangrove interior ponds, lakes and
creek areas select for the colonial morphs of Avrainvillea, not only by providing refuge habitats
from the intense fish-and-sea-urchin herbivory (Taylor et al., 1986) that is associated with open-
water systems (e.g., Littler et al., 1983; Lewis, 1986) but also by ameliorating the nutrient
stresses that frequently occur in such reef- and lagoon-ecosystems. This enables the more
delicate colonial morphology to prevail, spreading by means of the unique pseudo-rhizomatous
stipe structure (Fig. 25) to cover the otherwise unavailable flocculent anoxic peat substrate.
It is interesting to note that the mound formers, while capable of overtopping other
psammophytic (sediment dwelling) organisms, tend to bear prodigious quantities of epiphytes
such as Laurencia intricata, Cladophoropsis membranacea and Polysiphonia flaccidissima
(Figs. 12, 22), which, given sufficient light, would add about 30% to overall colony productivity
in this shallow light- and nutrient-rich environment (Fig. 23). An earlier study at Twin Cays
(Littler and Littler, 1985) recorded 17.2 and 13.4 grams of carbon fixed per square meter per
day at outer fringe, dense seagrass/algal, bay- and channel-sites, respectively. These values
rank among the higher productivity rates recorded and were two-to-three times the production
rates of the mangrove pond Avrainvillea colonies calculated in the present study. In contrast to
the epiphytized colonial morphs, the deeper occurring lagoon morphs have been shown (Littler
and Littler, 1999) to actively expel their more harmful epiphyte loads by translocation followed
by senescence and shedding (i.e., blade proliferation/ abandonment, Fig. 5).
The theoretical costs vs. benefits of coloniality in terrestrial plants and marine animals
(e.g., see review by Jackson, 1977) have received substantial attention. However,
consideration of this phenomenon for marine plants previously had been limited to the
advantages/disadvantages of the algal-turf morphology (Hay, 1981). In comparison to the
extraordinary mound-forming species of Avrainvillea, it should be noted that two other genera
of Bryopsidales also form knoll-like colonies. Caulerpa species, particularly the various forms
of C. racemosa, can overgrow reef habitats to create small (tens-of-centimeters high), but often
extensively spreading, humps. Halimeda is unique for the massive (tens-of-meters high) fossil
bioherms recorded (Drew 1997) from the Great Barrier Reef lagoon. Although time and
resources did not allow us to do comparative functional morphology studies on the two morphs
of A. nigricans (i.e., f. nigricans and f. spongiosa), we predict that the findings would have
closely paralleled those for the morphs of A. longicaulis and A. asarifolia.
Perennation
We also showed that the stipes and blades of the open-water morphs (Avrainvillea
longicaulis f. longicaulis and A. asarifolia f. asarifolia) indeed serve as expendable
assimilators, with a major function of building a massive perennating/storage organ, the columnar
holdfast (Fig. 11), which comprises the bulk of the thallus biomass (Olsen-Stojkovich, 1985).
Among all the other Bryopsidales, Avrainvillea is uniquely long-lived (see Littler and Littler,
1992) and does not undergo holocarpic reproduction (Clifton, 1997) leading to death. Physical
disturbances (such as storms and herbivory), as well as physiological stresses (such as epiphyte
loading), result in disproportionate losses of the relatively delicate expendable assimilators,
which can be readily replaced by perennation from the long-lived subterranean holdfast during
23
more favorable conditions. Selection for this strategy is amply represented in terrestrial
environments as shown by the multitude of vascular plants that crown sprout after physical
forces such as severe storms, fires, freezes or overgrazing have destroyed the above-ground
canopies. However, the only relevant marine example (Heck and Valentine, 1995) is the
seagrass Thalassia testudinum which is able to compensate for short-term grazing losses on
emergent shoots by mobilizing stored carbohydrates from the rhizomes (see Tomasko and
Dawes, 1989).
Ecological Role
The advantage of the deeply rooted morphs of Avrainvillea in open-water sedimentary
seagrass environments, such as Curlew Cay where the water column nutrients are consistently
low, lies in the fact that these plants can avoid physical catastrophic losses while tapping into the
much higher concentrations of interstitial pore-water nutrients (e.g., >200 µmol N, Williams and
Fisher, 1985). These findings add a further dimension to observations of nutrient-limited
productivity of benthic algae on tropical reefs (Kinsey and Domm, 1974; Kinsey and Davies,
1979; Smith et al., 1979; Hatcher and Larkum, 1983; Lapointe et al., 1987). Conversely, we
have shown that colonial adaptations of Avrainvillea that take advantage of high nutrient, but
anoxic, environments, such as commonly found in mangrove interior creeks, lakes and ponds,
result in some of the most prolific communities known. Documentation of such ecosystem level
differences in nutritional state and productivity, relative to the functional morphology of the
dominant primary producers, is critically needed in the construction of successful models of
benthic productivity for tropical marine systems.
ACKNOWLEDGEMENTS
We thank Vicki Funk, Jim Nix and Phil Taylor for field assistance. We are grateful to the
National Museum of Natural History’s Caribbean Coral Reef Ecosystem Program (CCRE
Contr. No. 686) for funding the field work. Additional funding for laboratory work was
provided by the Smithsonian Marine Station at Fort Pierce, Florida (SMSFP Contr. No. 590).
24
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