francois Michaud micho at
Mon Apr 8 14:05:37 EDT 1996

>From pecheux at (Martin Pecheux) 
Here we draw a general strategy to sample large foraminifers in reef 
monitoring stations, aims to guide local non-specialists to collect 
materials for a worlwide periodic survey, at a very few expense of work. 
This is the 3rd version of a working document (without plates) reread by 
several leader specialist of large foraminifers (Dr. P. Hallock, Dr. Erez, 
Dr. Lee, Dr. Rottger, Dr. Hohenegger, Dr. Venec-Peyre). People involved in 
reef monitoring are invitated to comment and critic before document 
finalization. And of course, as they will, to begin collection, perhaps 
first as described in "Simplified Sampling". See you all in Panama ! 

Goals are : assess long term reef degradation ; obtain a synoptic view of 
bleaching in large foraminifers ; acquire comprehensive data on global and 
temporal variability of ecology and CaCO3 production of those organisms ; 
and above all to have samples as soon as possible for future studies in a 
long term perspective. 
Those samples will also probably serve to monitor small foraminifers, 
ostracodes, micromollusks, bryozoans, etc... People interested in this 
perspective are invitated to contact us. 
Simple observations after sample collection are encouraged and are the only 
specialized work which might be done. Samples will be examined by our 
group, using classical technics and other such as high-resolution X-ray 
imagery. In any case, such samples will be valuable in a long-term 
perspective of monitoring reef healthiness. 


Long term monitoring of large foraminifers is becoming urgent with the 
general decay of reefs, often because of local causes in which pollutions, 
but also with the recent worlwide unexplained mass bleaching of reef 
photosynthetic symbioses, among them large foraminifers (Hallock and Talge, 
1993, Hallock et al., 1995, Pecheux, unpublished). They appear even more 
sensible to bleaching than corals, and they bleach before them or in years 
when corals do not (Hallock and Talge, 1993, Hallock et al., 1995). 
Moreover, it has been observed spectacular abnormalities of the shell 
associated with bleaching events, to a grade not known in geological time 
to our knowledge apart the Cretaceous/Tertiary boundary. This prooves 
irrefutably that bleaching is a new phenomenon, and of great significance 
at planetary level. 
This long term monitoring have been never undertaken, nonwithstanding its 
importance. Large foraminifers are very good bioindicators, and for 
exemple, comparaison of fauna composition between samples taken in 1974 and 
in 1989 in Mauritius was full of informations (Hottinger and Pecheux, in 
Why is it important to study large foraminifers ? 
- they are major reef CaCO3 producers, maybe the greaters. They are found 
in almost all reef biotopes, and are very important in mid to deep waters ; 
- they are easy to collect and store in great numbers in small samples; 
- they are excellent bioindicators of environmental changes, both by faunal 
composition and with shell biometrics ;  
- their reproduction, which is clearly pertubated now, is easy to monitor 
(size at reproduction and of embryo, number of offspring), and would be 
indicative for the whole ecosystem ; 
- they show a great diversity of shell types, biotopes, and algae 
symbionts. The old hyalin/porcellaneous divergence corresponds to quite 
different calcification systems, with different responses to carbon change 
- they are excellent experimental biological material, better than corals, 
easy to cultivate in great numbers, with indicative behavior toward/away 
light, agitation, temperature, etc. Their biology is best understood then 
of corals in some domains  ; 
- the geological knowledge on large forams is by far more complete than of 
any other reef taxon, given their abundance, dominance in some epochs, and 
their study by oil industry ; 
- also, there is a link with planctonic symbiotic foraminifers, among main 
ocean CaCO3 producers. 

The proposed sampling needs only very few hours works if integrated in 
normal procedure of reef monitoring (Coral reef monitoring handbook, Ref. 
Meth. Mar. Poll. Stud. 25, UNEP, 1984, Long-Term Global Monit., Pilot Proj. 
Mangroves Coral  Reefs, UNEP, 1991). Foraminifers are to be fully 
appreciated as main "other conspicuous organisms of interest". This 
monitoring will keep samples for future studies. In case of no standart 
corals monitoring, microfauna sampling such as here outlined is indeed the 
very best faster way for reef assessement. 
Samples susceptible to contain large foraminifers and already collected in 
reef for any other purpose, and particularly those before bleaching in the 
early 80's, are extremely valuable. They must be conserved with very great 
care. Even samples of beach sands can provide important informations of 
when did malformations began, one of our topic interrogations. 
In order to know disponibilities, it is asked to send a descriptif of those 
In a first step, some whole samples can be taken from your area (even as a 
"blind test"), dried and send to us for examination before further advice 
and collection. We recommand : 
- a sand beach sample, around 1 mm granulometry ; 
- an eelgrass sample (search a little white circles of Soritid, see below) ; 
- a turf/brown algae, shallow 1-3m depth crest or immediate front reef ; 
- sand and/or algae of your favorite, monitoring sites. 

There are two main objectives : a) collect regularly large foraminifers, 
both living and dead shells ; b) collect and observe living ones at and 
during bleaching or other pertubating events. Regarding efforts, minimum to 
better coverage is let to local people choice, and is indicated in order of 
priority by A) B) C). It corresponds to only few hours work if integrated 
with recommanded Coral Reefs Global Monitoring, otherwise to one half day 
work to a very great maximum of a week per year. 
Targeted genera are : 
A) Amphistegina, hyalin foram, because of its worlwide repartition and 
importance in sediment production, its shallow to deep euphotic habitat, 
lagoon to fore-reef, and various biotopes : algae turf, green-brown algae, 
eelgrass, sand facies, rubbles. 
A) Soritids (Sorites, Amphisorus, Marginopora) representing porcellaneous 
forams, easy to detect and observe underwater as white circles, epiphytic 
on eelgrasses, often abundantly in shallow facies. Whole sample with 
eelgrass must be conserved.  
B) porcellaneous Archaias, Cyclorbiculina (chlorophyte symbionts), 
Peneroplis (with generally rhodophyte symbionts), best encountred on algae 
in shallow facies up to tidal pool. 
B) Operculina/Heterostegina, either on soft or hard substrates, from 
surface (Caribbean, Pacific) or from 20 m depth (Indian) to deep euphotic 
B) Calcarinids in Western Pacific (Calcarina, Baculogypsina), which can be 
very abundant in near-crest shallow sand facies with water energy. 
C) Alveolinids, from very shallow to mid depth, with maximum abundance 
around 20-40 m depth. They are not well known, as their presence is 
generally detected only after examination of sand samples with lens or 
binocular, but might be the most bleaching- and pollution-sensitive genera. 
C) Deep flat species (Heterocyclina, Cycloclypeus). Their collection at 
50-150m depth usually requires a simple grab. Informations on them is 
desirable given the surface they inhabits in the world (~ 6 millions km2), 
and because they live in the most stable environment. 
First is the choice of 2 to about 10 sites rich in large foraminifers, 
which will be regularly visited (profitably where some samples have been 
collected in previous years). Locations will be know within some few 
meters, we insist. According to local assemblage, we recommand A) one 
-better two- backreef/lagoonal site, subjected to usual lagoon diurnal 
condition variation,  and one -better two- fore reef site, with rather 
stable environment, well bathed by open ocean water. They will be 2-5 m 
depth. Next priority is a 10-30 m depth scuba site on front reef, if 
present also in back reef B) then a multiplication of those sites, and C) 
one deep grab transect (maybe two if there are clear substrate differences) 
with 5-10 samples from 50 to 150m depth in clear water. Sites will be the 
most possible far away from local pollution source otherwise special cases. 
The sites have to be well caracterized (depth, light, often forgotten 
currents and water agitation, biological composition, desirable 
photographies) and homogenous at decadal meter scale, to minimize spatial 
variations. Aggregation of ~3 sub-samples within each site is recommended. 
Choosed biotopes will be :  
A) algae turf or brown or green algae field (Amphistegina and others); 
A) eelgrasses, with Soritids on leaves as well as Amphistegina and some 
other species, often at base or rhizome (which can be separated from upper 
part of leaves); 
B) sand facies, of 0.2-3mm granulometry, 2-5 m depth. Some samples of beach 
sands are indeed also wellcome, for completion of survey. 
C) rubble/boulder facies (Amphistegina,...), 2-5 m depth or deeper; 
C) very fine sand to mud facies (in both shallow protected areas and deeper 
The sites will correspond in general to permanent "Monitoring Plots" of 
inner/mid/outer lagoon, inner/outer flat, reef slope at 3 and 10m depth as 
outlined in Coral Reefs Global Monitoring.  
Samples on turf, eelgrasses or other algae have the very great advantage to 
collect only living forams. It is preferable to cut algae with scissors or 
knife in order to avoid sediment contamination, and take apart a sediment 
Usual standing crop is 1 to 10 specimens per cm2, up to 100/cm2 for highly 
productive biotopes (notably calcarenids in shallow reef flats). Samples 
will be considered sufficiently rich when few hundreds of living specimens 
are present. 
A constant sampling surface is mandatory. Usually a frame (often 10x10cm2, 
repeated three times with sub-sampling) is used, together with 
normalization to fresh or dry weight for algae biotope.  
After sampling in bags, algae are to be strongly agitated and frictionned 
as delicat cloth. Soritids on eelgrass have sometime to be detached with 
gentle brushing, sometime scrapped with knife. An other technique is to let 
the leaves in a seawater bac in darkness or mild-stress but aeration, and 
they detach by themshelves and fall on the bottom (but recuperation might 
be not total).  Conservation of rest algae dried samples is to be done. 
Boulders and rubbles must be brushed on their upper face and their lower 
face, and have also to be (very rougly) measured to know their develloped 
surface. Sandy bottom samples are best pick up with a transparent box or 
tube and a sliding cover to take only the very first half centimeter to one 
centimeter, otherwise very caefully by hand. Sample weight will range from 
less than one gram (corresponding for example to one thousand Amphistegina) 
to few hundred grams for sand or grab samples.   
In all cases, the residus are washed and slowly rinced with seawater to 
eliminate mud, light and organic particules, or algae. If necessary, 
sieving with a coarse mesh or strainer (0.5-1cm) will eliminate big 
fragments of material. Even if samples are rich in very fine sand, it is 
recommended not to sieve them (or only at 63u) to conserve juvenile 
specimens, as well as other small microfauna.  
Then samples are generally washed two-three time with freshwater (which 
induce protoplasm retraction) and then dryed on newspaper in air in the 
shadow. Alternatively, they can be conserved in 95% ethanol or buffered 
formalin, which keeps full colors of living protoplasm (buffering is 
important to avoid dissolution). 
They can seen with naked eyes (apart for the small juveniles), once one 
know what to search, often directly in the field when densities are high. 
Best examination is of course done with good lens (x12, better x20) or 
binocular at low magnification. 
Living forams display a full colored protoplasm, typical of the species, 
brown, green, yellow, purple, depending of type of symbiont. The presence 
of color in all but the last few chambers due to protoplasm retraction is 
commun and very caracteristic. 
A very usefull method to see living forams (and to sort them) is to let the 
sample in non-agitated seawater in a small bac, jam pot, etc..., preferably 
with a curved bottom as a salade saucer, with 2-3mm sediment, for one or 
more days, in dim light and with not too much temperature variations. Large 
forams will slowly climb (up to 10cm/day) for light and agitation on top of 
sediment and along the walls where they might be taken with the finger or a 
pincel. This examination is important for search of bleached moving 
specimens, otherwise easely confounded with empty shells. 
The samples taken during the selection of monitored sites will be kept and 
constitute a broad baseline allowing a possible ~ 10-20 years survey. It is 
recommended to collect numerosous samples (50-100) at this occasion for the 
same purpose, enough well localized, preferably on transects. 
The selected sites will be sampled : 
A) once a year in summer, at maximum temperature time, when standing crop 
and growth will be at maximum and yearly forms already adult, and with most 
probable bleaching ;  
B) once a year before spring, at minimum temperature, before reproduction, 
where some large forms are to be encountred ; 
Annual or bisannual survey are a "standart best-off". 
C) once in spring at time of rising temperature and weather change, and 
once in autumn. 
C) and/or two first priority sites might be sampled at the four seasons, 
with additionnal 3 times at spring, each month and half, for reproduction 
(many species reproduce once a year). 
Grab transect are worthy to be sampled only once (twice) a year. 
Special sampling associated with bleaching is the very more urgent, as are 
"episodic events" (UNEP 1991) Sampling must be undertaken as soon as coral 
bleaching is detected, then one week and one month after. Remember that 
large foraminifers appear more prone to bleaching than corals, and may 
bleach before or in years when corals do not, as in Florida 1992. One of 
our important question is if associations with symbionts other than diatoms 
are also subject of mass bleaching; abnormal orange color was observed in 
Cyclorbiculina (P. Hallock, com. pers.) and we observed high proportion of 
abnormalities in Sorites and Borelis. 
Observation under binocular for paling, mottling, bleaching, and of 
climbing behavior of white specimens (see above) should be systematic, and 
done on a fraction of collected samples. Other signs of stress is loss of 
mouvement and of adherence of living, well colored specimens, and presence 
of colored protoplasm in (only) the last chambers, before symbionts 
expulsion, and of course clump of expelled symbionts at aperture. This is 
the only analysis asked to be done by monitoring scientists.  Shell 
abnormalities can be also observed, or latter. 
Sampling just before bleaching event, said in few cases to be predictable 
within a week when dolldrum time set (B. Causey in Looe Key, Florida, in 
Williams and Bunkley-Williams, 1990, T. Goreau in Jamaica, pers. com.) is 
of course particularly wellcome. 
We are convinced that biological caracterization and long-term samples 
conservation for future studies are whorthy. Two main special monitoring 
might be done, for various delayed key biochemical and cytological 
caracterizations, particularly for bleaching at its start : 
- about one hour 14C/45Ca incubations ; 
- congelation and better liquid nitrogen storage. 
It is asked to signalize facilities for such possibilities. 
For completion of method description, here are recommendations for 
collection and transport of living specimens, in the optics of biological 
Large foraminifers are indeed quite resistant. Best is to collect them 2-3 
days before expedition. After standart collection, seiving might be 
usefull, both to eliminate small and big  particules (0.1-0.5mm and 5-10mm, 
depending on species), especially to get good sand water circulation 
therafter (sieving with a fine nylon mesh stocking is easy and fast). 
Then keep them in small bacs or aquarium to test their viability, and more 
important to sort them from the sediment and other microfauna , if culture 
conditions can be simply controlled (light from north window, temperature 
controller, air bubbling - better not from room where CO2 could be high- or 
aquarium pump agitator). 
The most important is that there must be low organic matters or algae, 
eliminated by carefull washing, nor meiofauna as mollusks, to keep pH in 
normal range (chemical buffers at 8.2-8.4pH might be used, or a 
NaHCO3-Na2CO3 mixture at 123mg-29mg/liter). In the container, forams and 
sediment must be not too thick (few millimeters) with 10-20 more seawater 
above. Temperature fluctuations are to be avoided as possible, although 
stressfull conditions are about lower 22oC and upper 30oC. Forams can be 
transported in plastic bags for few hours, or in bottle (even jam pot) 
during one day, sometime more, under room temperature. Best is to use one 
liter thermos bottle, kept in hand bagage if travel by air. If the travel 
does not exceed one day, it might be send through usual airplane postage if 
in 20oC-conditionned airplane luggage room, with accelerated transit if 
When convoyed, it is desireable to regularly gently shake the container 
each few hours, and change of seawater with clean one from an other closed 
jar, ideally with some air bubbling (each ~ half day at least) and exposure 
to low light in day. 
My advice to keep them long alive (I had Amphistegina reproducing for 5 
years in my kitchen) : blue light, some agitation and primarly high pH 8.5. 

On large foraminifers here is a list of publications for non-specialists : 

LEE JJ, 1995, Living Sands, BioScience 45/4, 252-260. A very good introduction. 
REISS Z, HOTTINGER L, 1984, The Gulf of Aqaba, Ecological Micropaleontology 
50, Springer Verlag Ed., 354p. With a very good long chapter on large 
forams, photo and drawning. 
HOTTINGER L, 1982, Larger foraminifera, giant cells with historical 
background, Naturwisssensch. 69, 361-371. Good presentation with different 
kinds of approach. 
HALLOCK P, 1984, Distribution of selected species of living algal 
symbiont-bearing foraminifera on two Pacific coral reefs, J. Foram. Res, 
14/4, 250-261, for kind of repartition and plate. 
HOHENEGGER J, 1994, Distribution of living larger foraminifera NW of 
Sesoko-Jima, Okinawa, Japan, PSZNI Mar. Ecol. 15/3-4, 291-334. Typical 
repartition (but >10 meters depth) and good photos. 

And concerning bleaching and shells abnormalities : 
HALLOCK P, TALGE HK, SMITH K, COCKEY EM, 1992, Bleaching in a reef-dwelling 
foraminifer, Amphistegina gibbosa, Proc. 7 Int. Coral Reef Symp. V1, 44-49. 
HALLOCK P, TALGE HK, 1993, Symbiont loss ("bleaching") in the reef-dwelling 
benthic foraminifer Amphistegina gibbosa in the Florida keys in 1991-92. in 
Global Aspects of Coral reefs: health, hazards and history. Rosentiel 
School Mar. Atmos. Sc., 8-13. 
HALLOCK P, TALGE HK, COCKEY EM, MULLER RG, 1995, A new disease in 
reef-dwelling foraminifera : implications for coastal sedimentation. J. 
Foram. Res., 25/3, 280-286. 

Large foraminifers are divided in two groups, those with an imperforate 
porcellaneous shell, composed of minute cristals which diffract the light 
and give them a white appearance, and those with a perforate hyalin shell, 
with big parrallel cristals transparent to light and a glassy aspect. Their 
internal space are divided in chambers and often chamberlets, and their 
internal structures are important to distinguish genera and species. 
As corals, they heavily rely upon photosynthesis of their symbionts, which 
are of various algae groups. They have active behavior, moving slowly with 
pseudopods toward elevation, light and agitation. Their life span ranges 
from few months, usually one year, up to four years at least (Marginopora). 
They reproduce mainly by multiple fission, giving 100-1000 small calcified 
embryos. Sexual reproduction give rise to a few percent of individuals with 
very tiny embryo ("microspherics") ordinarly with a very big size, 2-10 
times their clonal counterparts. 
They are main reef CaCO3 contributors, giving the surface they inhabits, 
95% of 6 millions km2 of reefs and tropical plateforms, producing up to 
2-3kg/m2.y for calcarenids, usually 100-500g/m2.y in shallow waters, and 
even 50-100g/m2.y in deep euphotic zone. 

Small (0.3-0.5, up to 1.5mm) helmet forms, purple color (rhodophyte 
symbionts) or green (chlorophyte symbionts in P. protea). Simple internal 
structure. Half a dozen species of Laevipeneroplis (=Peneroplis) and other 
similar genera (Spirolina, Dentritina), worlwide till subtemperate 
(Mediterranean). Mainly in very shallow water, on turf, algae or bottom, 
often in restricted facies subject to temperature, salinity and pH 
excursions (where shell abberations may be commun), and rare downto 60m. 
Disc (Cyclorbiculina, 2sp.) or helmet form (Archaias angulatus), about 2mm, 
up to 4mm, green (chlorophyte symbionts). Other similar genera (Broeckina, 
Androsina). Abundant in backreef shallow facies downto 20-25m, rarely in 
restricted facies (Androsina), on bottom or algae. Restricted to the 
Caribbean, but exist rare similar smaller forms in Indian ocean, New 
Large white discs, 2-6mm (Sorites 3sp., worldwide, Amphisorus heimprichii, 
Indopacific), up to 4cm (Marginopora vertebralis, western Pacific), with 
brown color (dinoflagellates symbionts similar to Symbiodinium 
microadriaticum, or green S. marginalis with chlorophyts). Sorites and 
Amphisorus mostly epiphytic on eelgrass where they are conspicuous, 
Marginopora generally dwelling on bottom. Mainly downto 30-40m, rarely 70m. 
Small (0.5-1.5mm) subglobular (Borelis pulchra, worldwide), elongate (B. 
sclumbergeri, Indopacific) to 5-10mm (elongate Alveolinella quoii, western 
Pacific). Brown diatom symbionts. Living in sand, sometime on hard 
substrate or algae, rarely seen during diving. Small Borelis can be 
shallow, mostly 20-50 m depth. 

HYALIN SHELLS (Rotaliina) 
Rather small (1-2mm) spheric, spheric with spines or stellate forms, brown 
(diatom symbionts). Apart Calcarina calcar (Indopacific), restricted to 
western Pacific where they are often very abundant (up to 100 
specimens/cm2) on sediments in shallow (less then 5-10m, rarely to 20m) 
high energy reef margin with current or bathed tidal pool. Also a small 
ecological Calcarina-like Asterigina carinata in Caribbean, somewhat 
Shape of lense with medium size (1-2.5mm), slightly assymetric, with brown 
color (diatom symbionts, also accessory chlorophyt ones). One genera, 
Amphistegina, abundant, with worlwide repartition. Shallow thick species 
(A. gibbosa, Caribbean, A. lessoni, A. lobifera, Indopacific) from surface 
downto 20-40m, then flatter A. radiata and deeper A. bicirculata, A. 
papillosa downto 150m. Inhabits various biotopes : most abundant in algae 
turf otherwise on shallow sands, well represented on green or brown algae 
as well as on eelgrass somewhat on the lower part, or on boulders, gravels 
on both upper and lower faces, or on mud-fine sand in calm or deep euphotic 
Mid-water and deep shelf species : 
- Operculina (and Nummulites)/Heterostegina : Spiral shell of 1.5-5mm, 
green or brown (diatom symbionts), thick in shallow waters, evolute in deep 
waters, 0 to 150m depth. O. ammonoides, rather on fine sand, mud or between 
eelgrass, H. depressa (Indopacific), H. antillarum (Caribbean) on hard 
substrate, boulders, dead coral head, coarse sand, sometime very shallow. 
- Heterocyclina/Cycloclypeus : Cyclical flat deeper water species, 5mm-5cm 
diameter (record 14cm), on sediments 70-150m depth where they can cover 
10-20% of the surface. Diatom symbionts. H. tuberculata in western Indian, 
C. carpenteri, Heterostegina operculinoides in eastern Indian-western 

MICHAUD francois 
Laboratoire de Geodynamique sous marine 
Universite Pierre et Marie Curie 
La Darse, B-P 48,  
Villefranche sur Mer, France 
Tel : (33) 93 76 37 40 ou 37 49 
Fax : (33) 93 76 37 66 
E-mail : micho at 

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