iCover Photograph: Cycloclypeusii

iCopyright © 2011 by The Kagoshima University Museum, Kagoshima
All rights reserved. No part of this publication may be reproduced in any form, electronic or mechanical, including
photocopy, recording, or otherwise, without prior written permission from the publisher.
For bibliographic purposes this publication should be cited as follows:
Johann Hohenegger. 2011. Large Foraminifera - Greenhouse constructions and gardeners in the oceanic microcosm.
The Kagoshima University Museum, Kagoshima. Bulletin No.5.
81 pp., 257 photographs, 8 figs.
ISBN 978-4-905464-00-6

Photograph on the reverse side: ParasoritesiiContents
Preface

vii

The originator of lens-shaped components

2

The body

6

Reproduction and life span

8

The gardeners

11

What’s the nature of these particles?

11

How does photosynthesis work?

12

Why plants have different colored pigments?

12

What’s the prof it for microalgae living in a foraminiferal test?

12

Which plants do the gardeners culture?

14

The cultivated plants

15

Red Algae (Rhodophyta)

15

Green Algae (Chlorophyta)

16

Dinoflagellates (Pyrrhophyta)

17

Diatoms (Bacillariophyta)

18

The construction engineers

20

The functional aspect

20

The building material 

22

The construction plan

24

The reproduction of greenhouse gardeners

35

The settlement of greenhouse gardeners

36Light

36

Temperature

36

Footing

37

The clans of gardeners

42

Purple gardeners (Peneroplidae)

42

Green gardeners (Archaiasinidae)

45

Blue to brownish-violet gardeners (Soritidae)

48

Ocher gardeners with spindle-shaped greenhouses (Alveolinidae)

50

Olive-green gardeners constructing lentil-shaped greenhouses (Amphisteginidae)

51

Ocher gardeners with star-shaped greenhouses (Calcarinidae)

53

Ocher to olive-green gardeners with large, often flat greenhouses (Nummulitidae)

60

The fate of empty glasshouses

67

The history of gardeners

71

－5－

－6－

Preface
This book is about microscopic organisms consisting of a single cell, which house microscopic algae asplants and thus construct complex greenhouses of calcium carbonate in tropical shallow water oceans. They
have a long geological history of about 350 million years. Today, their empty glasshouses are importantcomponents of carbonate sand in tropical shallow water, where they often attain more than 90 % of carbonate
sand grains. Beach sands in the tropical Indo-Pacific are named ‘living sand’ or ‘star sand’ according to theform of sand grains, which resembles to little stars or sun discs. The knowledge about life and demands of thesemicro-organisms to the environment is important for the preservation of carbonate sand beaches especially in theIndonesian Archipelago and the tropical West Pacific from the Barrier Reef to the Ryukyu Islands. Therefore, I
wrote this book in a non-scientific and, as I hope, generally understandable manner to focus the interest to theseorganisms and to the problems of preserving carbonate beaches.
There is a lot of institutions and people that helped me during my scientific work and supported themaking of this book. First, I have to thank the scientific and technical staff of the Tropical Biosphere ResearchCenter, University of the Ryukyus, Sesoko Station, making a 12 months stay in 1992/ 1993 (director the lateProf. Kiyoshi Yamazato) and a 4 months stay in 1996 (director Prof. Tazunori Takano) as an invited foreign
researcher possible. Second, I thank the Kagoshima University (president Prof. Hiromitsu Tanaka) for a 7
months stay in 1997/98 as a visiting professor at the Research Center for the South Pacific (director Akio Inoue)and for participation of a 4 weeks cruise in 1995 on the ‘Keiten Maru’ to Belau, where I got friendship withmany Japanese scientists, but was especially supported by Prof. Akio Hatta (Kagoshima University). Finally, I
will thank my good friend Prof. Kimihiko Ōki (director of the Kagoshima University Museum) for providing
support of the Japanese Society for the Promotion of Science for many stays at Kagoshima University and fororganizing a special cruise to Amami-Oshima, Tanegashima, and a flight to Okinoerabu Jima, where I could
take samples to broaden my horizon about larger foraminifera. Last, but not the least, I thank the Kagoshima
University Museum for publishing this book.
The Austrian Science Fund (FWF) supported investigations within several projects, where Elza Iordanova(3 projects) and Christian Baal (1 project) were employed. Franz Tatzreiter supported field work in 1996.
Discussions with Prof. Rudolf Röttger (Kiel) were useful for understanding the biology of these gardeners andmolecular genetic investigations of Maria Holzmann helped to clarify the evolutionary relationships between
different species.
All illustrations and most of the photographs were performed by the writer, otherwise the authors, almost
Christian Baal and Elza Iordanova, are cited. Finally, I thank M. Stachowitsch for correcting the English text.
Vienna, February 2010
Johann Hoheneggervii

It is a great pleasure to publish a book “Large foraminifera - Greenhouse constructions and gardeners in the oceanic
microcosm”. I became acquainted with Prof. Hohenegger at the fourth International Symposium on Benthic Foraminifera(Benthos ’90) in 1990. I stayed at Vienna University for study of benthic foraminifera at the northern most part of Adriatic
Sea for 7 months, 1994. At that time my family was under indebtedness to Professor Hohenegger and his wife. After that
Prof. Hohenegger stayed at Kagoshima University in 1995, 1996, 1997~1998, 1998, 1999, 2003 and 2004. He collectedbottom sediments and large foraminiferal specimens off Amami-oshima, Tanegashima, Amakusa-shimojima and Okierabujima in 1999, 2003 and 2004 with me. I would like to say thanks to a good friend Prof. Hohenegger for giving me thischance.

ŌKI KimihikoDirector of the Kagoshima University Museum

viiiGREENHOUSE CONSTRUCTIONS AND GARDENERS
IN THE OCEANIC MICROCOSMOS
What are the main components of this limestone?

Let’s have a look at one of the world’s most famous
cultural heritages, the pyramids of Gizeh! LocatedA closer look at the blocks shows a dense packing ofsouthwest of today’s Egyptian capital Cairo, the god-kingslens-shaped components measuring from 5 mm to 3 cm.

(pharaohs) of the first dynasties initiated the erection ofthese buildings as their mausoleums 4,500 years ago.
At 138.75 m (originally 8 m higher) the pyramid ofking Chufu (Cheops) is the tallest one. It was built on a
calcareous plateau together with the somewhat smaller
pyramid of king Chaefre (Chephren) and the much smaller
one of Menkaure (Mykerinos).

The base of the Cheops Pyramid. The mean height of thelimestone blocks is 1 meter.

These components consist of calcium carbonate (CaCO 3 )and are thus calcareous particles and pieces. Each of thesecomponents demonstrates a complex internal structure,
clearly visible in fractured pieces.
These structures hint to an organic origin, which is not
The Sphinx in the foreground with the pyramids of king Chaefre(Chephren) to the right and king Menkaure (Mykerinos) to the left.

surprising, because more than 90% of all limestone deposited
during Earth History originates from organism skeletons orshells.

The pyramid of king Chufu (Cheops).

While the sepulcher of the Cheops pyramid consists ofgranite blocks originating from quarries near Assuan morethen 600 km to the south, the pyramid itself is composedof large limestone blocks that had been crushed in nearby
quarries. Thus, the transport distance was not too far.

Details of a block from the Cheops Pyramid.

－1－

In the case of the pyramids, these lens-shapedof stony corals by arranging tiny calcareous minerals incalcareous components can be separated into 2 size groups.

different and complex order, leading to these structures.

The spaces between the larger components (size between

This gives rise to the question: what kind of organisms were

2 and 3 cm) are densely stuffed with lens-shaped grains

responsible for these lens-shaped calcareous objects in thecharacterized by sizes between 0.5 and 1 cm.

pyramid limestone and where did they originally live?
A further question relates to the function of thesecalcareous objects:a. Are these objects skeletons used to strengthen theorganism’s soft body to better resist mechanical forces,
much like stony corals do against the strong waves?
b. Are these skeletons used to enable movement
by stabilizing soft bodies, like the exoskeleton(surrounding the soft bodies) of insects or theendoskeleton (within the soft body) of vertebrates do?
c. or can these objects be regarded as shells to shelter
the organism against the environment, by enablingthem to retract the body into the shelly cave, like clams

The surface of a block from the Cheops Pyramid showing thecomposition of the limestone by small, lens-shaped components of
5 mm size and larger lenses with 30 mm size.

and snails do?
To get answers to these questions, we have toinvestigate these objects in detail.
One investigation method is to make sections of a single
object. There are two preferred orientations for sectioning alens-shaped object, leading to two types of sections.
The first preferred orientation corresponds to thesymmetrical plane dividing the lens-shaped object into two
equal parts. This plane, called the equatorial section, is
unique; no other equatorial section is possible (Figure 1).
The second preferred orientation, perpendicular to
the equatorial section, runs through the center of the lensshaped form. The line, which is oriented perpendicular

Isolated calcareous lenses (Nummulites perforatus Montfort)
falling into two size groups (photo C. Baal).

to the equator and runs through the center, is called theaxis of rotation; such sections are called axial sections.
As opposed to the equatorial section, which is unique, anthBefore the rise of biological sciences in the 17 century
and knowledge about fossilization, which means theinfinite number of axial sections are possible by rotating
360° around the axis.

preservation of organic material or skeletons and shells in

Making equatorial and axial sections for the smallerrocks or stones, farmers regarded the smaller components

and the larger lens-shaped objects reveals their structures

as ‘petrified lentils’ and some people called the large ones

and demonstrates similarities and differences between both

‘petrified coins’. Therefore, today’s scientific name for thesegroups. In equatorial sections of both lens-shaped objects,

components is ‘Nummulites’, originating from the Latina chamber is located in the center. This chamber is large inname for small coins, which is ‘nummulus’, and the Greek

the group of small-sized objects and extremely small in thename ‘lithion’, which means ‘stone’.

group characterized by large objects.
Starting from this center, a series of chambers is

The originator of lens-shaped components

arranged in a spiral following the equatorial plane. ThisWe know that organisms can form complex hard

type of coiling is named planispiral. It can be found in

structures like vertebrate bones, shells of clams, or skeletons

living cephalopods, which are related to squids, protecting－2－

Figure 1. Preferred sections on a planispirally enrolled shell (foraminiferal test after Carpenter 1858).

－3－

Equatorial section through a lens-shaped object (size = 12 mm;
photo C. Baal)

Equatorial section (size = 30 mm) of a shell with a small initialchamber and many whorls (photo C. Baal).

Axial section through a lens-shaped object (size = 7 mm; photo
C. Baal)the soft body within beautiful shells (Nautilus), as wellas in their fossil relatives, the ammonites. When spiral

Equatorial section (size = 8 mm) of a shell with a large initialchamber and a few whorls (photo C. Baal).

coiling leaves the equatorial plane and moves continuously
along the axis of coiling, then it is named trochospiral.

threads, which are interconnected much like a spider’s

Trochospirally coiled shells are typical for snails.

net. Each test contains only a single cell. Therefore, these

Squids and the Nautilus live in the sea. This is whereindividuals belong to the group of single-celled organisms

we can also find relatives of the objects that produced thelike amoebas. Similar to the latter, they do not have a fixedshells that make up pyramid limestones. They are muchbody shape like other single-celled organisms, but cansmaller in size than the Nautilus. Another difference is thechange their flexible body, especially in the outer part, forlife habit. While cephalopods swim about (nektonic), theselocomotion and feeding. These flexible parts create different

smaller organisms live on the sea floor. Living on the sea

foot-like forms, which are called pseudopods.

floor is called a benthonic or benthic habit.

Dissimilar to the amoebas, which move slowly by

The bodies themselves make up the second difference.

forming rounded pseudopods (lobopods), the threadlike

Cephalopods are multicellular animals characterized by ainterconnected pseudopods are called reticulopods. Besides

set of organs like eyes, jaws, intestines, execratory organs,movement, reticulopods function as organs for nutrition

gonads, and different numbers of tentacles.

by catching food and transporting it into the inner cell in a

The small-sized organisms living on the sea floor

process called ingestion.

do not show such differentiation. From the opening ofIn the early 19 th century, when the first of these

the shell or test, these organisms spread a bundle of fineorganisms were described as living forms from the sea－4－and as fossils, they were regarded as ‘cephalopods’
because their tests or shells bore a certain similarity. True
cephalopods with a chambered shell ( Nautilus and the fossil
ammonites) connect their chambers, which are filled by gas
for buoyancy control, with an organic string called ‘sipho’.
This creates complex chamber connections. In contrast,
test chambers of these single-celled organisms are filled by
the cell body and the connections between chambers are
simple openings. This led the famous paleontologist Alcide
Dessalines d’Orbigny (1802-1854) to differentiate between‘Céphalopodes siphonifères’ (which means ‘carrying
a sipho’) and ‘Céphalopodes foraminifères’ (’carrying
a foramen = opening’). Today, the term Foraminifera
remained, including all single-celled organisms living(mostly) in the sea, hiding their soft cell bodies in tests andproducing reticulopods as organs for movement and foodcapture.

Side and frontal view of a Nautilus shell with planispiralenrollment (photo P. Pervesler).

Trochospiral enrollment demonstrated by the land snail
Achatna (photo P. Pervesler).

A living Nautilus − a relative of squids − with large, but simple
eyes and many tentacles for catching food.

A living Peneroplis (size = 1.2 mm) with pseudopods spreadingfrom the test opening (aperture).

－5－

respiration by various transport mechanisms.
The liquid within the cell is called cytoplasm andconsists of water (80-85%), in which organic molecules likeamino acids and proteins (10-15%), lipids (2-4%), sugars(0.1-1.5%) along with inorganic molecules and ions (1.5%)
are dissolved.
Organic molecules of higher complexity regulate life
within the cell. Proteins as the most important structuresof life mainly act as structural components. They canalso accelerate processes by transforming simple molecules
into larger ones, or, vice versa, disassemble complex
Shell of the cephalopod Nautilus (size = 15 cm) cut close to
the medium section, demonstrating the body chamber and gas
chambers. The body chamber is connected with the embryonicchamber by a tube called siphon (photo P. Pervesler).

molecules into simple ones. This group of proteins is
known as enzymes. Another important group of proteins
are responsible for molecule transport. All these processes
need energy.
Proteins as chains (macropolymeres) of amino acids
are assembled at ribosomes, which are tiny grains found inlarge numbers within the cyctoplasm.
Since proteins cannot be synthesized chaotically allover the cell like in bacteria, especially when these cells
are as large as in foraminifera, regulation is necessary.
This involves formation and transport of proteins andother organic and inorganic substances at places where
they are needed at the moment. Therefore, the inner cell

Shell of Peneroplis (size approximately 2 mm) showing
the different chambers that are connected by simple openings =foramina (drawing by Carpenter 1855-1860).

is not a large undifferentiated bottle, but is structured bymembranes, the so-called endoplasmatic reticulum, wheremost ribosomes are concentrated.
Beside organic macromolecules, which are synthesized

The bodyin the cytoplasm, organic and inorganic substances thatForaminifera consist of a single cell (Figure 2).

are needed outside the cell membrane for protection or

The normal size of foraminifera is between 100

movement are assembled in separate compartments calledmicrometers and 2 millimeters, which is large for single-

dictyosomes. Membranes surround these dictyosomes.

celled organisms. Sizes of other single celled organisms

In one group of foraminifera, tiny calcite-needles 0.5 andlike diatoms (siliceous algae) or dinoflagellates are much

2 micrometers long are formed in dictyosomes and thensmaller, ranging from 10 to 100 micrometers. Most bacteriatransported within so-called Golgi vesicles to the cellare distinguished by a size that is one order of magnitude

surface.
The reversed mechanism takes place during ingestion ofsmaller, between 1 and 10 micrometers.
The foraminiferal cell representing the whole

food like bacteria, microalgae or organic waste (detritus).

individual is separated from the surrounding water byFeeding is necessary to obtain organic macromolecules anda membrane. Organic molecules related to the group ofthen disassemble them into more simple organic molecules.

fats (phospholipids) construct these membranes. These

This process is termed digestion. Simple organic molecules‘fatty’ membranes prevent mixture of fluids between bothlike sugars, organic acids, and lipids can now be usedmembrane sides. In the case of foraminifera, sea water

to assemble larger macromolecules that are specific andfrom outside the cell cannot be mixed with fluids of thenecessary for the organism. Parts of the cell membrane,

inner cell. The membranes do, however, enable penetration

where food is captured, invaginate. This gives rise toof smaller molecules like oxygen and carbon dioxide forbladder structures, the phagosomes, where food is digested.

－6－

Figure 2. Scheme of a foraminiferal cell (modified after Campell and Reece 2008).

－7－

All processes for assembling and disassemblingplanktic life is to reduce test density by incorporating lipids

substances need energy. Energy is gained by respiration,(fats). This helps keep the tests in the upper 200m of therepresenting the one part of metabolic processes that iswater, where the animals feed on phytoplankton.

typical for animals. During respiration, higher organic

Today, siliceous algae － the diatoms － represent themolecular structures, mainly sugars and fats, are burnedmajor part of the phytoplankton in the sea. Planktic diatoms

with the help of oxygen into inorganic carbon (carbon

are the main food of planktic foraminifera, much likedioxide). The regained energy is chemically bound inbenthic diatoms are the main prey of benthic foraminifera.

ATP (adenosine triphosphate), where it can be used

Living diatoms as food sources, however, are found only inwhenever necessary. Respiration takes place in separate cellthe sunlit uppermost parts of the oceans: they need sunlightcompartments called mitochondria.

as an energy source to transform carbon dioxide and water

All life processes performed by proteins have to be

into carbohydrates. This metabolism process is known as

regulated by a special structure, where the information

photosynthesis. The uppermost water column allowing

about protein structure and the onset of protein construction

photosynthesis is called the euphotic zone. Benthic

is stored. Except bacteria, this information in the form offoraminifera living below the euphotic zone cannot feed on

nucleic acids (DNA = Deoxyribo Nucleic Acid) is bundled

living micro-algae, but have to use the products of organic

as chromosomes within the cell nucleus. The nucleus isdecay, the detritus.

separated from the other cell parts by a double membrane,
allowing regulated penetration of information carriers in the

Reproduction and life span

form of proteins into the nucleus and by mRNA (messenger
Ribo Nucleic Acid) to the outside.

Foraminifera have a complex life cycle with twoalternating generations (Figure 3).

The cell wall of the foraminifer is not strengthened

One generation is characterized by a single set ofby organic macromolecules like structure proteins or

chromosomes (where the information as DNA is stored)

polymer sugars as in other single celled organisms, wherethat is restricted to the nucleus. Organisms with a single set

they lead to a fixed and unchangeable cell form. Rather, itof chromosomes in the cell nuclei are called haploid. The

demonstrates plasticity due to the flexible cell membrane,

haploid generation of foraminifera is named ‘gamonts’

where proteinaceous microfilaments allow changes inbecause a single gamont produces hundred thousands ofshape by contraction.

gametes by multiple fission of the cell nucleus.

Furthermore, the cyctoplasm of the foraminifera

Gametes of foraminifera are small (1.5-2.5μm),

is differentiated into a dark inner part of the cell, thepossessing 2 or 3 flagella for active motion to find anotherendoplasm, and a transparent outer part, the ectoplasm.

gamete as a partner for fusion. Sexual differences of

While most organelles are located in the endoplasm,

gametes like sperm and egg cells are not known; gametes

making it nontransparent, the ectoplasm is responsible forof a foraminiferal species originating from different

test construction.

individuals have the same form and are thus called

A net-like bundle of reticulopods is spread from theisogametes.

ectoplasm, which consists of filamentous and contractible

After fusion of two gametes, which unifies thecyctoplasm strings. The main task of reticulipods is foodchromosomes in one cell nucleus, the new individual

capture, movement, and test construction.

(zygote) possesses the double set of chromosomes.

Foraminifera lack flagellae (like in human sperm cells)

Organisms with a double set of chromosomes are so-or cilia (like in Paramecium) that function as organs for fastcalled diploid organisms. Although the zygotes arelocomotion, which are typical for active swimmers. Instead,extremely small, because they result from a fusion of twothey live preferably on the sea bottom, moving slowly on or

nuclei and very little additional cell plasma, the cells can

within the sediment and gathering food. When foraminifera

become larger than the gamonts before reproduction. This

live in the water column as passive swimmers (plankton),generation is named ‘agamonts’ because they reproduce

they develop special mechanisms like globular tests andasexually.

long inorganic spines to increase frictional resistance. This

The multiple fission of diploid cell nuclei is combined

reduces their sinking velocity. Another way to adapt towith a reduction fission (meiosis) of the chromosomes. This

－8－

Figure 3. The life cycle in larger foraminifera (size of gametes not to scale).

－9－yields a lesser number (several hundred) of young gamontspossessing the single set of chromosomes (haploid)
compared to the enormous number of gametes in sexual
reproduction.
Reproduction by multiple fission and meiosis normallytakes place within the foraminiferal test. The young
gamonts remain within the parental test and grow until they
develop the first 3 to 4 chambers. After forming the test, thegamonts are released into the seawater.
Every young gamont get parts of the parental
cyctoplasm containing all organelles like mitochondria thatare necessary for the life of young gamonts.
Since young gamonts are sheltered by the parental test
until they grow large enough, survival of a young individual
released to the seawater is much higher compared to theextremely small and naked zygote. In the latter case, before
conjugation, the tiny and naked isogametes have to find apartner, which must not originate from the same parental
cell (hindering self-fertilization). Although hundreds ofthousands of gametes are released by a single gamont, it isextremely difficult for a gamete to find a partner originatingfrom another gamont.
Low settlement densities cause difficulties because
they hinder fusion of gametes when distances are too far todetect a partner. Another difficulty is the non-contemporary
release of gametes in most foraminifera. Since the survival
time of free gametes is restricted to a few days, differencesin gamete release of more than one day makes conjugationof gametes originating from different parental organisms
improbable even if they may live close together.

The foraminifer Neorotalia (size = 2.5 mm) with broken broodchamber and hatched offspring.

The much higher survival rate of young gamonts(compared to the difficulties in finding a conjugation partner
for the small isogametes) explains the strong abundance
differences in both generations. Adult gamonts are thus
much more abundant than agamonts. The proportions
between generations depend on the species, but vary from
1 agamont per 100 gamonts down to 1 agamont per 1000
gamonts in larger foraminifera.
The life span of generations differs between and within
the species. It ranges from 2 weeks to 1 month in planktic
foraminifera, where the individual sinks during this period
from the sea surface down to 200 m. After attaining the
maximum depth, planktic foraminifera reproduce sexuallyand the tiny young forms, possessing a few chambers,passively rise to the surface due to their low weight.

The foraminifer Amphisorus (size = 40 mm) with 4 rings oftransparent brood chambers and hatched offspring.

Foraminifera living on the shallow sea floor have a life－10－

span between 2 and 6 months, whereby diploid agamonts

What’s the nature of these particles?

often live longer than haploid gamonts. Reproduction

Investigation by high-resolution microscopes using theperiods depend on season, whereby the first reproduction

TEM (transmission electron microscope) has shed light onin spring is caused by high food availability during thethe nature of these particles.

bloom of marine microalgae (phytoplankton). High input oforganic food and inorganic nutrients due to rainy seasons,when plant debris is swept into the sea by rivers, also
promotes reproduction in shallow tropical and subtropicalseas.
The life span of deep-sea foraminifera depends on theorganic input by the phytoplankton bloom in spring and isthus longer than in shallow-living foraminifera, normally
about 1 year. This is caused by a slow-down of life
processes that saves energy.

The gardeners
Foraminifera living today in shallow water arecharacterized by sizes that often considerably exceed thesize of normal foraminifera (100 micrometer to 2 mm).

Transmission electron microscope (TEM) image of a symbiotic
microalgae (size = 0.0048 mm) within a foraminiferal cell. The
chloroplast (P) responsible for photosynthesis surrounds thenucleus (N) and the mitochondrium (M). A large vacuole (V) is
typical for storing the products of photosynthesis like glycerols andlipids (from Leutenegger 1984).

While some groups grow to about 4 mm, other forms havetests that measure a few centimeters; the largest species

Every particle is separated from the cytoplasm of

today attains a size between 4 and 12cm. Thus, larger

the foraminifer by a membrane. It possesses an own cellforaminifera are truly the largest single-celled organisms

nucleus along with so-called vacuoles, which are large

living today!

spaces for the storage of substances that are surmounted

Beside the cell characters described above, whichby membranes. These cells also contain special laminatedcan be found in all foraminifera, the larger foraminiferaorganelles that are not found in the cytoplasm of normal

also have intensively colored organic grains measuring

foraminifera. These intensively colored organelles, named

between 4 and 20 micrometers. While the cytoplasm of aplastids or chloroplasts, are typical for plants cells because’normal’ foraminifer is uncolored or has an extremely weak

they are necessary for photosynthesis.

brownish color, these tiny particles within the cytoplasm

Therefore, every pigmented particle within theare responsible for an intensive coloring that is visible incytoplasm of larger foraminifera is a single-celled

every living larger foraminifer.

organism that is capable of photosynthesis. According

Based on this color, the identification of larger
foraminifera as living individuals is easier compared toto the extremely small sizes, these organisms are calledmicroalgae.

’normal’ foraminifera, where differentiation between

The life form of microalgae within a larger foraminifer

empty tests and living individuals is difficult (because inis known as symbiosis. Here, the larger foraminifer acts

those living foraminifera the tests are filled with more oras the host and the small single-celled microalgae are theless colorless cyctoplasm). Two methods are available toguests.

identify ’normal’ foraminifers as living individuals. The

In symbiotic life, both partners have to obtain profit.

first requires looking for activities. If pseudopods are not

What’s the profit for the host by housing microalgae

visible, the foraminifera have to be killed and then thewithin the test instead of eating them? To understand this,cytoplasm made visible by special colors (i.e. Rose Bengal).

we have to look at the kind of food that microalgae produce

This method is not necessary for living larger foraminifera,

and that foraminifera can use (instead of simply digesting

because they are naturally colored through the above-

the whole microplant).

mentioned small particles.

－11－How does photosynthesis work?

phycobilin.

Plants cells have the capability to transform water (H 2O )Color differences in the thalli or leaves depend on theand carbon dioxide (CO 2 ) into simple carbohydrates,

absorption of light of different wavelengths. Red lightmostly sugars, which are a balanced combination of carbon,

with long wavelengths, which is best absorbed by green-hydrogen, and oxygen. This process needs energy that iscolored pigments, penetrates the atmosphere down to thegained from the sunlight. The chemical reaction is written

Earth’s surface. Nonetheless, the sun’s wavelengths changeasin the sea. The low-energy red light is rapidly absorbed　　　　 sunlightin the uppermost surface water, while high-energy blue-n (H 2O ) + n (CO 2 ) ⇒　 n (CH 2O ) + n (O 2 )green light with short wavelengths penetrates down toand is called photosynthesis (φωϛ = light, σ ú ν θ ε σ η

150 m in clear ocean water. In these deeper parts, light= combination). In a first step of photosynthesis, simple

is best absorbed by brownish to purple-colored pigments

sugars known as glycerols (for example glucose with thesuch as those represented in chlorophyll a, chlorophyll c,formula C6H12O6) are synthesized and later transformed

fucoxanthin, and phycobilins.

into more complex carbohydrates. Such compounds

Therefore, multicellular plants living in the sea

include starch grains (found in potatoes) or cellulose, which

are distinguished near the ocean water surface by thestrengthens the walls in plants cells.

dominance of green-colored organisms, like sea grass andMost single-celled algae produce, in a first photosynthetic

green algae (for example the well-known sea salad Ulva). A

step, much more glycerols or fats (lipids) than necessarytransformation from brownish to red colors is characteristic

for the life processes of the small algae. Sometimes, up tofor deeper-living algae (red and brown algae).

80% of the glycerols and lipids are not used by the algae and

The single-celled organisms with chloroplasts that serve

released into the surrounding medium. When this medium

as symbionts for the larger foraminifera also show theseis the foraminiferal cytoplasm (instead of seawater), thentendencies. Larger foraminifera working as gardeners andthe foraminifer can directly use these excess glycerols andliving at different depth have to utilize this capability oflipids as food. This ultimately yields energy by respiration,

their photosynthetic plants.
Therefore, the foraminifera work as gardeners at

making the forminifera independent from capturing food.

different depths in illuminated areas of the sea floor.
Why plants have different colored pigments?

They have to culture those plants adapted (that grow best

Photosynthesis starts with the transformation ofsunlight into chemically bound energy. These processes areor produce a maximum of glycerols) to specific lightwavelengths.

performed within the chloroplasts by the use of pigments.
Pigments are of different color. The pigment mostly
used by plants is chlorophyll b , which is characterized

What’s the profit for microalgae living in a foraminiferal
test?

by an intensive green color. The related pigments

Beside carbohydrates as energy resources necessary forchlorophyll a and chlorophyll c have colors ranging fromlife processes, all organisms, even plants, need inorganic

brownish ocher to bluish to olive green. Other pigments,

molecules to synthesize complex organic macromolecules.

like xanthophyllids, phycobilins and carotins, are

The most important elements are nitrogen (chemical symbol

characterized by brown to purple to red colors.

N), phosphorus (P), and sulfur (S).

While most higher plants like mosses, ferns, herbaceous

Nitrogen is an important element in amino acids.

plants, grasses, and trees have an intensive green color

Proteins are chains of amino acids having different lengths

in their leaves due to the dominant chlorophyll b, lower

and structures. Nitrogen is also an important element inplants like multicellular or single-celled algae show

organic bases in nucleic acids, which are responsible fora variety of pigments in their cells or thalli (leaf-likestoring (DNA) and transporting (RNA) information to

structures in multicellular algae) and thus have different

those places where the synthesis of inorganic or organic

colors. Especially the large brown algae get their color

substances via proteins takes place.

from xanthophyllid pigments, mainly fucoxanthin. The

Phosphorus is important in all cell membranes because

purple color of the red algae is based on the pigment groupthey consist of phospholipids. Nucleic acids (DNA and－12－RNA) also need phosphoric acid, and phosphorus is anwater because of missing nutrients. Therefore, clear andimportant element of the energetic reservoir ATP (adenosine

blue ocean waters dominate in the tropics and subtropics,

triphosphate).

because light penetrates the surface water without being

Sulfur is an important ingredient in some proteinsabsorbed by inorganic and organic particles. These oceans

and coenzymes (functioning together with a protein as anregions are called ’blue deserts’ based on their lack of richenzyme),organic life.

Beside these main inorganic elements, metallic elements

Only along the west coast of continents in thelike magnesium (Mg ), potassium (Ka ), calcium (Ca ), andsubtropics, where trade winds transport the warm surface

iron (Fe ), as well as trace elements, are also essential forwater westwards towards the ocean center, does cold

life.

and nutrient-rich deeper water surge up to the surface.

Land plants get these important inorganic nutrients

Phytoplankton life is extremely rich in these ’upwelling’

from the soil through roots by taking up water. Inorganic

regions, making room for abundant animals that feed either

nutrients are either completely dissolved in the soil water,on the phytoplankton and multicellular plants, or feed onor they are bound as complex molecules like ammonium

smaller animals. Upwelling regions are thus the best fishery(NH 4 ) and nitrate (NO 3 ). Most of these molecules represent

sites.

disaggregated products of higher organic molecules by

Coastal shallow waters on the east side of continents inanimal digestion (catabolism). They cannot be used in

the tropics and subtropics are not nutrient-depleted when

the further production of the organism-specific organic

rivers transport nutrients into the sea, especially during

macromolecules.

the rainy seasons. Otherwise, coastal regions in the arid

When farmers or gardeners culture plants they therefore

zone, where deserts are developed on the continent, lackneed to provide sufficient inorganic nutrients. Especiallythis nutrient input by rivers. Correspondingly, the shallow

plants growing in monocultures require large amounts ofwaters here are depleted in inorganic nutrients. Thesenutrients. Therefore, human gardeners and farmers fertilize

regions are found mainly on the eastern side of continents.

the soil either by dunging and manuring or by applying

Examples include the Red Sea to the east of the Nubianartificial fertilizers.

Desert or the northeast coast of Australia.

All plants living in the sea can take up these nutrients

Shallow waters around tropical islands that are locateddirectly from the seawater. Most nutrients are transported

far from the continent are also characterized by poor

into the sea by rivers, explaining the rich algal presence ininorganic nutrients. This is because rivers cannot bring incoastal areas.

enough nutrients from the island, although these islands

On the other hand, nutrient uptake is more difficult for

may have dense tropical vegetation.

plants living in the upper 150 m of the sea, when the sea

Thus, unicellular as well as multicellular plants livingbottom is below 200 m. Ocean floors, however, lie between

in the sea have difficulties surviving in ’blue deserts’ and2000 to 4000 m. Here, waste products of catabolism sinkmust develop alternate strategies to inhabit these regions.

to the bottom and cannot be used by the single-celled

Living as symbionts in a host, for example in stony corals,

phytoplankton living in the upper 150 m, where light isgiant clams or a larger foraminiferal cells, provides the

not absorbed and photosynthesis is possible. Because

microalgae with inorganic nutrients, which are directly

phytoplankton does not have 3000-m-long roots to takeobtained from the host as waste products of its digestion.
A further profit for the plant as one partner of theup nutrients from the sea floor, other mechanisms have to

symbiosis is the availability of the inorganic carbon

provide them with nutrients.
In polar and subpolar regions of the oceans as wellnecessary for photosynthesis. Land plants get inorganic

as in ’normal’ temperate seas, vertical mixture of coldcarbon directly from the air, which is rich in carbon dioxide.

with warm waters transports nutrient-rich bottom waters

But marine plants have difficulties because carbon dioxide

to the surface. This is not the case in the subtropics andis dissoluble only in cold, acidic seawater. In the alkaline

tropics. Here, no mixture of the water masses occurs, andtropical warm surface waters, this molecule is transformed

warm surface waters constantly overlie the cold deeper

into the unstable carbon acid (H 2CO 3 ), which is dissociatedwaters. Phytoplankton is extremely poor in such surface

instantly into hydrogen (H＋ ) and carbonate (ＨＣＯ ３－ ) ions.

－13－

Therefore, warm temperate and tropical surface seawater isrich in hydrogen carbonate (ＨＣＯ ３－ ) and carbonate (ＣＯ ３２－ )ions, which can be used for the calcification processes ofskeletons and shells in animals and plants:

Ｃａ ２＋＋２ＨＣＯ ３－⇔ＣａＣＯ ３＋ＣＯ ２＋Ｈ ２Ｏ
During the calcification process of the foraminiferal
test, the second inorganic carbon ion that is not bound in the
calcium carbonate can be directly used for photosynthesisby the microalgae. This process explains the continuous
production of calcium carbonate skeletons of organisms
housing symbiotic algae. This may result in enormous
skeletons on a macro-scale (stony corals, giant clams) as
well as on a micro-scale (larger foraminifera).
Therefore, larger foraminifers as gardeners provide
their culture plants with inorganic nutrients and carbon ionsin ’blue deserts’, where they can grow and reproduce. The

Details of the last chambers of Planostegina, where single
small microalgae return to the final chambers after being disturbed.

Which plants do the gardeners culture?

foraminifer gains profit from the plants by obtaining food in
the form of simple sugars, or by feeding these plants in case

There are three requirements for a gardener:
The first requirement is the size of the plant.

of starvation.

The plants have to be small-sized for transport
between different test parts. Connections
between the chambers of the foraminiferal test
are often extremely small. The smallest are at
4μm (=0.004mm), allowing only the smallest
microalgae to pass through. All foraminifera
retract their cytoplasm to the inner test parts incase of unfavorable conditions of the surrounding
seawater. The cytoplasm is then spread to themarginal chambers when conditions become
normal.
This requires the symbionts to move throughsmall connections between the chambers during
cytoplasm retraction and spreading. Only tiny,
single-celled microalgae fulfill this condition.
The second requirement is to know which plant
grows and reproduces best in the environment inwhich the foraminifer lives.
Conditions for best growth and reproduction
are, on the one hand, optimal wavelengths for theplant to photosynthesize. On the other hand, theplant has to get enough inorganic nutrients likenitrogen, phosphorus, and sulfur for constructing
higher organic substances. This requires thegardener to serve these inorganic nutrients to the

The foraminifer Planostegina (size = 3 mm) from 90 m depth withretracted protoplasm, which is colored by symbiotic microalgae.

－14－

plant.

the appropriate symbiotic algae by specific enzymes.

How do foraminifera acquire the plants?
The easiest way is by asexual reproduction. After

After recognition as a symbiont, so-called lysosomes,

multiple fission of the foraminifers’ cell nucleus into several

i.e. membrane-surrounded bobbles carrying digestive

hundred nuclei, every nucleus is surrounded by parental

enzymes, do not conjugate with the phagosome carrying

cytoplasm containing all necessary organelles. This process

the microalgae (because in the case of conjugation thealso splits the symbiotic algae such that every young

microalgae will be digested). The membrane separating theforaminiferal cell obtains a few symbiotic algae; these algae

algae from the foraminiferal cytoplasm originating from thethen become the base of the new plant stock of the growing

phagosome is named symbiosome.

foraminifer.
The cultivated plants
Let’s have a look at the different plants the larger
foraminifera can decide to harbor:
Red Algae (Rhodophyta)
The first group of marine algae fulfilling these
conditions belongs to the group of Rhodophyta, the redalgae. Normally, red algae are multicellar plants of different
size, growing up to 50 cm. The Corallinacea , a group of red
algae, show strong calcification between their cells and are
Reproducing Amphisorus (test diameter = 40 mm) withnumerous 2-chambered offspring.

responsible for strengthening the skeletons of dead coralbranches: they cement both the small and large interspaces
between these branches. Therefore, the stability of thereef crest of coral reefs is based mainly on cementation bycoralline algae.
Not all red algae necessarily have a red color originatingfrom the photosynthetic pigment group phycobilin: otherpigments like chlorophyll a and chlorophyll c are present
within the red algae in different proportions, leading tobrownish or even dark green colors.
Only a single red algal species named Porphyridium

purpureum fulfills the requirements for becoming a
symbiotic microalgae in foraminifera. This is because thewhole individual is a single cell. The size ranges from
5 to 6μm. The pigment phycoerythrin of the plastids, a
Hatched Amphisorus (size = 0.15mm) incorporating small
symbiotic algae originating from the parental organism.

phycobilin, is responsible for the plant’s intensive purple

This transfer is not possible in sexual reproduction,light with short wavelengths, which penetrates downbecause gametes do not have enough space for organelles

to 200m in clear ocean water. Therefore, Porphyridium

outside the cell nucleus, and certainly no space forpurpureum works best in energy-rich, short wavelengths.

symbiotic algae. Therefore, the young diploid agamonts

On the one hand, short wavelengths are dominant inhave to pick up free-living algae from the seawater anddeeper water because red light with longer-wavelengths

ingest them by phagocytosis.

is absorbed at the water surface. On the other hand, thecolor. Phycobilins reflect red light and absorb blue-green

The foraminifer must then decide which ingested

foraminiferal test also absorbs long wavelengths throughmicroalgae can be used as symbionts, and which are

special test structures in extremely shallow water. In thisutilizable as food. The decision process is based oncase, only short wavelengths － meaning blue green light －biochemical reactions in which the foraminifer recognizes

penetrate the test.

－15－

Unlike in other symbiotic microalgae, the symbiosome
membrane does not surround Porphyridium purpureum.
Reproduction of Porphyridium purpureum is always
asexual through multiple fissions.
Superfluous photosynthates in the form of glycerols
are spread into the surrounding medium, but the amount ofglycerols is apparently not very high. Therefore, feedingon glycerols produced by red algae is insufficient for theforaminiferal host. The foraminifera culturing this plant
have to capture additional food for themselves and also toprovide the microalgae with inorganic nutrients.

Green Algae (Chlorophyta)
Members of only one genus within the single-celledgreen algae are used as symbionts in larger foraminifera. All
species of the genus Chlamydomonas possess two flagellae
in free-living forms, which allows active movement in
the seawater. The size is about 10 micrometers and theflagellae are approximately the same length as the cellbody. Reproduction in free-living Chlamydomonas is
asexual by multiple fissions and sexual by conjugating
isogametes, which look identical to normal cells. There are
no morphological differences between gametes and normal(vegetative) cells.
Possessing the pigments chlorophyll a and especially
Light microscope and TEM image of the single celled red
algae Porphyridium (diameter = 0.0036mm). The chloroplasts (P)dominate the cell, where 2 stark grains (S) and mitochondria (M)are visible (from Lee 1990).

chlorophyll b in the plastids allows green algae to absorb
red light. Therefore, larger foraminifera can use them onlyin the shallowest sea as “cultures” because photosynthesis
in deeper regions, i.e. below 40m, becomes difficult as red
light is absorbed in the upper parts by water molecules.

Living Dendritina (size = 1.2 mm) colored by the purple
symbiotic microalgae Porphyridium.

The single celled free living green algae Chlamydomonas (bodysize = 0.015mm) possess 2 flagella for active movement.

－16－

Dinoflagellates (Pyrrhophyta)
These microalgae are very abundant in the oceans
today, representing a high proportion of the phytoplankton.
The single-celled individuals possess two flagella, whichallows active movement in the water. While one flagellumis responsible for movement, the other surrounds the celllike a girdle, stabilizing the cell during movement.
Why do these small plants need a girdle flagellum
for stabilization? This is based on the grotesque formof the cells, which is caused by various cellulose plates
TEM micrograph of the endosymbiontic green algae
Chlamydomonas (diameter = 0.008 mm). Cup shaped chloroplasts(P), the nucleus (N), Vacuoles (V) and stark grains (S) are visible(from Leutenegger 1984).

covering the cell body. These plates give dinoflagellates
the appearance of armored individuals. Free-living
dinoflagellates differ in size and form. Chlorophyll a and c
are the main pigments in the plastids, allowing a range ofcolors from ocher to olive green and bluish, but never theintensive green of chlorophyll b.
Many animals living in the tropics use one group of
dinoflagellates as symbionts. Especially organisms withstrong calcareous skeletons or shells (that do not move orare more or less fixed to the sea-bottom like stony corals or
giant clams) exclusively use dinoflagellates as symbionts. In
these cases, the microalgae do not inhabit the cell plasma,
but live within the tissue of the multicellular organisms.
The beautiful color of stony corals or the shell edges of the
giant clam originate from the different pigment colors ofthe microalgae.

Living Parasorites (size = 4 mm) colored by the green
symbiotic microalgae Chlamydomonas.

The absorption of light by the olive- to bluishcolored pigments chlorophyll a and c is profitable forphotosynthesis in deeper environments, but absorption in

Chlamydomonas loses the flagellae within thethe shallowest waters is also possible. Like in humans,

foraminiferal body because active movement is unnecessary

permanent exposure to UV-irradiation causes cancer.

in the host. Reproduction of Chlamydomonas within the

Dinoflagellates can decompose the highest-energy UV-light

cell is always asexual by multiple fissions.

into harmless wavelengths using special proteins, much like

The carbohydrate mannitol released by Chlamydomonassun blockers for the human skin. They therefore protect the

into the surrounding medium is a combination of sugar andgenetic material of the host, which is concentrated in thealcohol. The proportion of superfluous photosynthates that

nuclei, from this dangerous light. This enables foraminifera,

are released into the foraminiferal cyctoplasm is not high.

corals and giant clams to live in the shallowest sea directly

Therefore, the foraminifera housing green algae have toexposed to the sunlight.
Since dinoflagellates are the dominant symbiont grouptake up additional food.
Furthermore, Chlamydomonas cells are characterized

within multicellular animals, they received the nameby a large amount of starch grains, again a carbohydrate,

zooxanthellae, a combination of animal (zoon = ζώον) andstored in special vacuoles. The foraminiferal host uses these

the yellow color (chansos = ξανσοσ). The zooxanthellae

grains either by dissolving the protective cell membrane oflose their cellulose plates when living in the foraminiferal

the microalgae and digesting only the starch grains or bycell or in animal tissues. The naked cells keep their flagellae

totally digesting the tiny plants.

for active movement within the tissue or cell, but they often
lose these organelles, especially when active movement is－17－

unnecessary. This is the case when the zooxanthellae are
passively transported by the cytoplasm.

Living Amphisorus (size = 3.8 mm) colored by the
dinoflagellate symbiotic microalgae Symbiodinium.

The zooxanthellae produce mainly fats (lipids)
as superfluous products of photosynthesis, which are
The dinoflagellate algae Symbiodinium is used as a microsymbiont in many invertebrates like stony corals and giant clams(mean body size = 0.012 mm).

released into the foraminiferal cyctoplasm; glycerols
are less important than in the red and green algae.
Although the proportion of photosynthates that are set
free is higher (~25%) compared to red and green algae,
larger foraminifera and all multicellular animals housing
dinoflagellates have to take up additional food forrespiration and to synthesize complex organic molecules.

Diatoms (Bacillariophyta)
These small organisms are the most abundantmicroalgae in today’s oceans, representing the highest
proportion of phytoplankton. Thus they are the main
primary producers - this means that inorganic carbon as
represented in carbon dioxide is transformed into organiccarbon in the form carbohydrates in the oceans. Diatoms
also live on the sea floor. They can cover the bottom with
TEM micrograph of the endosymbiotic dinoflagellate algae
Symbiodinium (diameter = 0.007 mm). Chloroplasts (P), thenucleus (N) with chromosomes, vacuoles (V) and the base offlagella (F) are visible (Leutenegger 1977).

mats in the shallow seas, where light penetrates to the sea

Zooxanthellae are much smaller than free-living

material (silicic acid). Diatoms living on the sea floor

dinoflagellates, with sizes ranging between 4 and 20(benthic diatoms) possess frustula in the form of shoeboxes,

micrometers. Most zooxanthellae belong to the genus

whereas the planktic forms are distinguished by frustula

Symbiodinium . Larger foraminifera share a single

that resemble hat boxes due to their circular form.

floor and enables photosynthesis there.
The single-celled individuals protect their cell bodies
with box-like shells, called frustula, consisting of siliceous

Symbiodinium species with stony corals and giant clams,

The size of a diatom cell is not constant, but changes

while the remaining two Symbiodinium species arecontinuously in becoming smaller during asexual

restricted to larger foraminifera.

reproduction. Maximum size is between 10 and 100

Reproduction in Symbiodinium seems to be asexual in
the foraminifera, since sexual reproduction has not yet been

micrometers, making them useful as symbionts in larger
foraminifera.
Pigments of the chloroplasts in diatoms are similarreported.
－18－

tropics, an optimum of about 2000 Micro-Einstein is
attained during summer noon. The absorption of lightintensities through water particles in clear ocean water
reduces light intensities to 10 Micro-Einstein at 150 m
depth during summer noon. Some diatoms prefer these low
light intensities, which means that they grow best under
extremely low light intensities.
This advantage of partitioning the whole photic zone
by diatoms preferring distinct light intensities makes
them the ideal symbiotic microalgae, especially for larger
foraminifera. As opposed to other algal groups, where only

Free living diatoms of different size.

a single genus (the red algae Porphyridium, the green algae
Chlamydomonas, and the dinoflagellate Symbiodinium) isused as an endosymbiont, several genera and species ofdiatoms can be used by larger foraminifera. This depends
on the restriction of diatoms to different light intensities.
Larger foraminifera that prefer extreme shallow water haveto use other diatoms as endosymbionts than foraminifera
living in quiet water with low light intensities. This isproblematic for those gardeners that try to cover a wide
range of light intensities, living from close to the surface
Scanning electron microscope (SEM) micrograph of afrustulum ( = shell) of a diatom (size = 0.022 mm) attached to aforaminiferal shell.

down to the deeper, light-depleted parts. Such gardeners

to dinoflagellates, consisting of chlorophyll a and c, butshallow zone, and changes to symbionts preferring lower

lacking the green chlorophyll b. Ocher to ocher-greenish

light intensities when inhabiting deeper parts.

have to change the plants. The same species is able toharbor diatoms preferring high light intensities in thecolors predominate in diatoms, allowing photosynthesis

Diatoms used as endosymbionts by larger foraminiferawith high-energy blue-green light, which is absorbed

do not need frustula for protection, thus they are naked.

by these pigments. Diatoms are the only phytoplankton

Transport within the foraminiferal cyctoplasm is passive

group that photosynthesizes under extremely weak light.

because the diatoms lack mechanisms for active movement.

While all other phytoplankton is restricted to the so-called

Reproduction is always asexual by simple fission. Since

euphotic zone, where the depth limit is round about 150 m

the endosymbionts are not restricted by a frustulum, theyin clear, tropical ocean water, diatoms show a positive

maintain their size during the series of asexual reproduction.

photosynthetic rate (i.e. the proportion of organic carbon

Normal size is between 4 and 10 micrometers.

gained through photosynthesis is higher than the loss

Since they are not longer enclosed by a frustulum, they

through respiration) down to 250 m. This zone between

can change their form, allowing them to pass through the

150 and 250 m with extremely weak light is called thesmallest chamber connections with a minimum diameterdysphotic zone.

of 4 micrometers. The different genera and species can be

Especially diatoms living on the sea floor demonstrate

identified by setting the diatoms free and culturing them on

different grade of dependence from light intensities.

an appropriate medium. The free symbionts suddenly build

This means that they reproduce best under specific light

frustula, enabling their identification based on the highly

conditions. Some diatoms prefer the high intensities founddiverse forms of frustula. Representatives of the genera

near the water surface. Light intensities are measured in

Fragilaria, Achnanthes, Cocconeis, Amphora, Entomoneis,

Micro-Einstein, counting the number of photons striking

Navicula, and Protokeelia have hitherto been described.

a standard area. These intensities change due to seasons,More are expected in the future as research on these micro-

geographical latitudes and the day-night cycle. In theplants progresses.

－19－all the demands for the life of the foraminifer. Therefore,
glasshouses have to be convenient and simplify the life of
the host as well as allow the ‘gardener’ to cultivate ‘plants’.
Second, the building material of glasshouses isimportant, on the one hand for strengthening them against
destruction by water movement, and, on the other hand,for making parts of the walls transparent to enable the light
penetration necessary for the ‘plants’.
Third, constructional aspects are important to enableaccommodation of the glasshouses to the environment
and fulfilling all functional demands. Basic constructional
TEM micrograph of an endosymbiotic diatom (diameter =0.008 mm). Chloroplasts (P), mitochondrium (M), the nucleus (N)and the large vacuoles (V) are visible (from Leutenegger 1977).

plans exist in foraminifera; they have to be modified bythe ‘gardener’ to fulfill the functional requirements forcultivating plants.

The functional aspect
The function of the construction has two main points.
The first is to protect the gardener against the environment,
hindering being eaten by predators or becoming infectedby bacteria or viruses. Large predators can be snails,
scaphopods, and fishes, which all consume the wholecytoplasm; examples of small predators that attack only
parts of the foraminifera are small worms, predatory
relatives (other smaller foraminifera), or ciliates (relativesof Paramecium).
The second point is to allow connections between the
Living Amphistegina (size = 3 mm) colored by symbiotic
diatoms.

cell body inside the test and the surrounding seawater,
enabling the transport of nutrients and metabolic products.
The construction must also be conducive to regulating theDiatoms release the highest amount of produced

metabolism within the test and to providing the microalgae

photosynthates (40 to 80%) into the surrounding medium.

with necessary nutrients in an optimal way. This makes test

These photosynthates consist mainly of lipids (~50%)

openings and connections between test parts important.

and glycerols (~10%). Therefore, the foraminiferal host
becomes independent of additional food, and food uptake

Construction openings
There must be a number of openings between theis often restricted to the necessary uptake of inorganic

inner part of the construction, where the foraminifer lives

nutrients.

and retracts under unfavorable circumstances, and the

The construction engineers

outside, allowing the penetration of the cytoplasm to form

Larger foraminifera acting as gardeners have to use

reticulopods.

their houses to protect themselves against the surrounding

The primary role of these foot-like structures inworld, but also as cultivation greenhouses for their ’plants’.

‘gardeners’ is to attach the construction to a base, which canTherefore, beside gardeners, they can also be regarded as

be stones, broken and dead coral peaces, sea grass leaves,construction engineers.

or thalli of sea weeds. Therefore, additional elements

Three general principles are important for all

improving the fixation of pseudopods to the substrate aredeveloped around the openings, or these openings areconstructions, and thus also for microscopic glasshouses:
First, the constructions must be functional, fitting

subdivided or multiplied. The fixation of a glasshouse－20－

is always temporarily; thus, under poor conditions likeon the excessive photosynthates produced by the plants.

low light intensities or inadequate substrate, the larger

Otherwise, uptake of a small amount of food is always

foraminifer can move to more appropriate places.

necessary for gardeners to provide ‘micro plants’ with

Beside this possibility to change localities, it becomesinorganic nutrients like nitrogen and phosphorus. To obtain

important to dig into or out of the sediment, for example

enough food in large-sized tests (>1 cm), many openings

sand (grain size between 0.063 and 2 mm) or silt (0.0039

for the penetration of reticulipods are necessary to increase

to 0.063mm). Gardeners living on coarse sand sometimes

the chances for food capturing.

dig into the sediment to stabilize the construction. In fine-

Therefore, the number, form, and position of openings

grained sand and silt, digging below the surface helps

allowing penetration of the cytoplasm depends on theprotect the gardeners against predators. When strong storms

necessity for fixation to the substrate, movement on or indislodge gardeners from hard substrate or transport themthe sediment, and food capture.

in sands, they become suspended in the water column likeother sediment grains. This means they are transported byConnections within the construction

the storm currents and ultimately buried in the sediment.

Since chemical reactions during metabolic processes

In such cases, the foraminifers have to dig out of the sandare improved in small, delimited volumes of the cytoplasm,

using their pseudopods.

constructions that enclose large cytoplasm bodies have to

The second role of the reticulopods is to capture

be divided into smaller units. These so-called compartments

food. Some ‘gardeners’ need this type of food (either

are separated by walls. Connections between compartments

living microalgae or organic remains known as detritus)

are thus important for the directed cyctoplasm flow.

additionally to the nourishment they get directly from theGas molecules like the oxygen necessary for respiration

symbiotic ‘micro-plants’ by digesting them or feeding

are transported by that flow to the mitochondria,
where ATP-molecules, the energy units, are produced.
Subsequently, these energy-carrying molecules have to betransported to those sites where substances are synthesized,
because any synthesis requires energy. The carbon
dioxide resulting from the respiration process has to betransported to the plants, which can directly use them forphotosynthesis.
The information transfer by chemical signals fromthe environment or any compartment of the glasshouse to
the command centers (nucleus), and vice versa, requires a
regulated cytoplasm flow within the complex construction.

SEM micrograph of Dendritina (scale bar = 0.1 mm) showing
multiple test openings (apertures).

This calls for an organized system of openings connecting
the small compartments to enable the shortest route of
information flow between any compartment of the cell andthe regulation center.
A further important function of the construction is toallocate the algae into an optimal position for gathering
light, a prerequisite for photosynthesis. A wide space
just below the glassy windows has to be supplied forthe microplants, enabling them to attain optimal light.
Additionally, tiny caves called ‘egg-holders’ help fixationof microalgae just below and partly within the test wall.
This protects the symbionts from the cytoplasm flow in the

SEM micrograph of Amphistegina lobifera (scale bar = 0.1mm) showing a structured aperture.

compartment centers.

－21－

humans － allows the formation of different skeletons andshells, like the complex frustula of the diatoms, because
it can crystallize in an amorphic manner (opal) without
preferred crystal axes. Unfortunately, in surface watersof tropical and temperate oceans, organisms can only use
silicic acid as an endoskeleton. There, organic cytoplasm
in single-celled organisms (like diatoms and radiolaria) or
tissue in multicellular organisms (like sponges) protect themineral from the aggressive seawater. Silicic acid dissolves
in contact with the alkaline seawater that dominates theMicro-Computer Tomography of the last chambers ofOperculina that are connected by foramina (F) at the base of
the septa separating the chambers and by stolons (S) randomly
distributed on the septal area (photo A. Briguglio).

surface ocean waters in warm climates.
The basic material of skeletons and shells used by mostorganisms in warm, alkaline seawater is therefore calcium
carbonate (CaCO 3 ). The basic module of the foraminiferal
test consists either of a single, tiny crystal of calcium
carbonate. It can also consist of foreign particles, which
are taken up from the surrounding sea bottom, fixed by anorganic or inorganic cement, then by a calcareous cement.
The latter wall structure is similar to concrete material,
where stones are also fixed by calcareous cement resulting
in compact and firm test walls. The use of organic cements

Sectioned initial chambers of Operculina (scale bar = 0.1 mm)
showing “egg-holder” structures at the inner chamber surface,where the symbiotic algae are positioned and thus protected fromthe foraminifers’ protoplasm (SEM micrograph by courtesy of L.
Hottinger).

yields more flexible test walls.
Calcium carbonate is not amorphic like opal (SiO 2 )but crystallizes along three preferred axes. Light striking
perpendicular to the crystal surface is non-refracted onlyin the direction of the optical axis; otherwise it is refracted
due to the high refraction index of calcium carbonate.

The building material

This is important for the construction of transparent wall

The basic material of constructions like greenhouses

structures. Since the single calcium carbonate crystal usedmade by humans is not restricted to a single type. Any

by foraminifera for wall construction is extremely small (1building is composed of various basic materials such as

to 5 micrometers), the transparent walls necessary for theboards, blocks of stones, bricks, concrete or other types

glasshouse effect can be obtained through extremely thinof construction material. Most greenhouses constructed

walls consisting of only a few layers of calcium carbonate

by humans consist of iron or wooden beams and girders,

crystals. In another strategy, transparency in thick walls is

where large glass windows close up the inner part ofpossible when the tiny crystals are arranged with all optical

the greenhouse and protect it from weather conditions.

crystal axes oriented perpendicular to the test surface.

Allowing the penetration of sunlight creates an inner

Not all basic modules for test wall constructions

climate, whereby different blinds regulate the intensity ofdeveloped by foraminifera in their long geological history

sunlight that reaches the plants.

can be used by larger ‘gardening’ foraminifera. One

Similar to the buildings erected by humans, thecondition for the test wall is their composition of calcium

foraminifera are not restricted to a special type ofcarbonate crystals. Because warm surface seawatersmaterial as basic modules, but use different minerals forare depleted in carbon dioxide, the synthesis of calcium

constructing test walls. The best material for constructing

carbonate by the foraminifera improves photosynthesis

transparent tests should be silicic acid (SiO 2), which isof the micro-algae by providing the necessary inorganic

used by various organisms as skeletal material. Silicic

carbon ions during the calcification process.

acid － the main component of glass windows made by－22－

Today, such larger gardeners use only two types of basic

modules. Both ’bricks’ are based on calcium carbonate

the crystals are filled with organic material, allowing the(CaCO 3 ) in the modification known as calcite. They

penetration of gas molecules like oxygen or carbon dioxide.

differ, however, in their content of additional magnesium

Therefore, no special openings for the interchange of gases

carbonate (MgCO 3 ), which is incorporated in the crystal

during respiration are necessary. Second, the complete

lattice of the mineral. A proportion of magnesium up to 4%

disorder of the thousands of optical axes leads to a total

is called low magnesium calcite, while high magnesium

light refraction and reduces the penetration of light throughcalcite can have a content of 23% magnesium.

thin test walls.

According to these two types of minerals used in test

On the inner and outer surface of the test wall, thewall construction, foraminifera working as greenhouseneedle-shaped crystals lose their disorder. Here, a different

gardeners can be differentiated into two groups. Besidetype of crystal is produced. It results from the ordereddifferences in the crystals, the formation of these ‘bricks’ －arrangement of crystal needles parallel to the surface anda process termed biomineralization － also differs.

from fusion into larger units. The resulting arrangement issimilar to a parquet floor, with the same smooth surface but
on a micro-scale! This means 10,000 times smaller then the‘Bricks’ of high magnesium calcite
The single crystal is needle-shaped, where the opticalwooden parquet floor in human rooms and halls!

axis corresponds to the longitudinal axes of the needle. Its

The total reflection of light in combination with alength is between 1 and 3 micrometers, but each foraminifer

completely smooth surface gives these tests the appearance

using this type of crystal retains a constant length in allof porcelain coffee cups at the microcosm level.

crystals. If a foraminifer uses crystals of 1.3-micrometer

This condition allows ‘normal’ foraminifera withlength, then all crystals used for the test wall are of thatporcellaneous walls to live exposed to extreme sunlight,

precise length. The diameter of the needles can varyfor example in the shallowest seas of the tropics and warm

between 0.4 and 0.6 micrometers but is also kept constanttemperate seas. This is because the test wall protects

within one species.

the foraminiferal cell from the injurious UV-light. The

Needles are formed within the foraminiferal cell ingreenhouse gardeners with this wall structure must

dictyosomes and then transported through ‘Golgi-vesicles’

construct stable tests, where light can penetrate throughto the site where a new test wall has to be formed.

the test walls. They therefore regulate light penetration by

The arrangement of these equally sized needles inthinning the test walls at those test parts where the micro-

the wall is completely irregular and chaotic. This isplants are concentrated. This yields enough light for theadvantageous in two ways. First, the interstices between

symbionts but protects the foraminifera’s genetic material.
It does this by keeping the cell nucleus, or often a bundle ofnuclei, in shadowed areas protected by the thicker test walls
or in the center of the test.
‘Bricks’ of low magnesium calcite
The single crystal is extremely small and can differ
in size. The wall is formed by an ordered arrangement ofsmall crystals to larger crystal units. Within such a unit,
all crystals have the same orientation of the axes and theirsurfaces are in contiguous contact, with no interspaces
between the crystals. Therefore, gas exchange between
both sides of the wall is impossible and special openings－ so-called pores － have to be constructed to enable gas

SEM micrograph showing the broken test of the porcelaineous
foraminifer Quinqueloculina (scale bar = 0.001 mm) withirregularly ordered calcite needles of the inner wall and thesmoothed surface caused by plate-like needles arranged like aparquet floor (photo C. Baal).

exchange.
Low magnesium calcite crystals and crystal units are
not formed within the cell in dictyosomes, but crystallize ina space bordered by two organic layers, which form the new－23－

while globular tests have a simple rounded opening. These
test openings are called apertures.
Again, a few foraminifera leave those single-chambered
tests when they grow larger. They briefly live naked likeamoebas, grow, and then construct a new test adapted totheir new size.
Most foraminifera overcome this problem of testleaving during growth by adding a larger chamber to theolder test part and keeping the connection between the
SEM micrograph showing the transparent (hyaline) test
wall of the foraminifer Ammonia (scale bar = 0.001 mm) broken
perpendicularly to the surface with blocks of ordered calcite
crystals. Gas exchange between the outside and inner test isprovided by pores (photo C. Baal).

chambers by openings, the foramina. These foramina are
the former apertures in simple tests. In most foraminiferawith tests, growth leads to chambered forms, whereby thebasic chambers can be either tube-shaped or spherical.
Differences in the geometrical order of chambers
during growth lead to an extreme variety of test forms.
Straight tests are constructed when consecutive chambers
are arranged along a straight or slightly curved line. These
tests are at a disadvantage in environments with high waterenergy or sediment motion because they can easily break.
Therefore, rounded and more stable test are constructedby different modes of chamber sequence. The arrangement
can be irregular like a ball of string (streptospiral).
More commonly it coils in a plane (planspiral) like thecephalopod Nautilus, or coils in conical form along an axis

SEM micrograph showing the surface of the transparent(hyaline) test wall of the foraminifer Operculina (scale bar = 0.001mm) demonstrating the density of pores.

(trochospiral), comparable to snails.

chamber wall. The inner layer acts as the starting place forsurface area that enables light penetration for their plants

the crystallization, and growth of the crystal units continues

through broad ‘windows’. This is especially important in

until the second layer terminates crystal growth.

deeper regions, where light is weak.

Starting from this basic construction plan, the gardeners－ as architects － have to build greenhouses with a large

When all optical axes of crystal units are oriented

A solution to this problem is to construct large and very

perpendicular to the surface, incident light can pass in athin, flat tests that exhibit a high proportion between cell

non-refracted manner through thick test walls. Even thicksurface and volume. Additionally, these constructions havetests are completely transparent. This so-called hyaline

to be separated into small, equally sized compartments－

wall structure is preferable for gardeners living in deeper

but with large windows－to support biochemical processes

regions, where light is weak for photosynthesis by theduring metabolism.
How can this be done, considering the restriction

microalgae. At those light-depleted regions, the gardenersof possessing only the above basic construction plans?

develop special light-intensifying structures.

Should a series of chambers be built step by step in an

The construction plan

irregular manner, or arranged in a coiling plane, or arranged

Although a few foraminifera － some of them live inalong a coiling axis? The first and the third solution are

freshwater lakes － do not develop tests in which to hide,

inappropriate for constructing flat tests, leaving only athe vast majority construct tests of various forms and sizes

single solution: planispiral enrollment - coiling around an(Figure 4).

axis in a coiling plane (Figure 5).

The basic elements of tests are single tubes or spheres.

The simplest solution is to start with the first chamber,

Tubes are either open at both sides or closed on one side,

the proloculus. All succeeding chambers are arranged step－24－

Figure 4. Tendencies in foraminiferal test construction.

－25－

Figure 5. Different ways to construct large tests originating from an planispirally coiled test.

－26－

by step around the first chamber in a plane, forming aspiral. After an initial increase of chamber size in the firstfew whorls, these sizes will be kept constant during further
growth. This allows the development of compartments
constant in size, but needs an extremely long period of
growth. Because of the constant chamber height, themathematical spiral called ‘Spiral of Archimedes’ canmodel the test outline.
This simple way to construct a glasshouse iscomplicated by a functional aspect explained above, namely
the connections between compartments. The step-by-step
growth makes the former aperture of the last chamber,the original connection to the surrounding seawater, into
a foramen (the opening between the next-to-last and the
new last chamber). Accordingly, foramina are the only
connections between chambers, and the aperture is the
single connection to the surroundings. This makes the paththat information and transport has to take from the outside
to the central test and vice versa extremely long. This also

X-Ray micrograph of Operculina ammonoides (size = 2.5 mm)with a test following the spiral of Archimedes.

hinders a time consistent distribution of information andespecially for the large Nummulites specimens exceedingtransport over the compartments.
Therefore, this ‘simple’ construction method restricts

10 cm in diameter.

gardeners and architects to small tests (like Peneroplis
pertusus).

Another construction plan allows faster test growthby constantly increasing chamber heights. The outline ofLarger and giant glasshouses were made possible by thisthe test follows a so-called ‘logarithmic spiral’, also foundmethod after the invention of a so-called ‘canal system’.

in fossil and recent squids that have a shell like the living

The invention of this thermion system located within

Nautilus or fossil ammonites.

the test wall makes the gardeners into plumbers as well.

Growth of chambers with straight septa involves

These tubes represent a complicated system of connections

weakness in the peripheral part due to the large space.

between the chambers, allowing much shorter and direct

Such chambers can be easily fractioned by predators like

communication between chambers and the outside.

fishes or even through friction by larger sediment particles

In contrast to pores, where only gas exchange isduring intensive water motion. A backward bending of

possible, the cytoplasm can flow through these canals.

chambers has a strengthening effects: the distances between

This allows the transport of larger molecules like proteinsconsecutive chambers remain constant along the wholeor carbohydrates (sugar polymers), of synthesized organic

chamber height, which adds mechanical strength to theparticles and even symbionts. Therefore, in case of danger,

peripheral test parts.

the whole cell plasma can quickly be retracted into theinnermost test.

This construction plan allows faster growth to largesized tests, and connections between chambers do not

Building new chambers step-by-step is a time-necessarily require additional connections like a canal

consuming and tedious process, and continuous addition

system. Otherwise, single foramina at the chamber baseof chambers is impossible. After adding a new chamber,allow a short and direct connection from the outside to thethe foraminifer has to rest and take up inorganic nutrients

center, but peripheral chamber parts are less well provided.

by feeding. Accordingly, test sizes of more than 2 cm takeMultiplication of apertures along the front of the last

several years. For very large individuals from the geologicalchambers leads to multiple foramina connecting consecutive

past, such as those that make up the stones of the Egyptianchambers; this guarantees consistent information andpyramids, a life span up to 100 years has been estimated,

product transfer to all cell parts.

－27－

SEM micrograph showing the canal system within the wall andsepta of Nummulites (scale bar = 0.1 mm). The test is dissolvedby acid, while the empty space of chambers and the canal systemrunning in the wall and septa was filled by resin cast and thus
remained.

Logarithmic spiral of Peneroplis (size = 1.5 mm) with bended
septa.

units. Since a chamber is formed during a single growth
process, a series of chamberlets representing the single
chamber is constructed during this short growth process.
Such an amplification of equally sized compartments isless time consuming than the step-by-step procedure in the‘Spiral of Archimedes’.
Besides test strengthening, the construction of smaller
compartments simplifies metabolic processes in thesesmaller units. To provide the prompt and short transferof substances between compartments, a complex systemof openings between chamberlets has to be established.
These openings do not originate from former apertures
Logarithmic spiral of Operculina (size = 3.5 mm) with straight
septa.

and are therefore not called foramina but stolons. Since
an information transfer from and to the regulation center
becomes very complicated in such systems, the cell nucleus

This construction plan is the oldest one for obtaining－acting as the regulation center－is subdivided into manylarge flat tests. It has been reported for the first time in the

nuclei. This yields short distances from the multiple

Jurassic ~ 190 million years ago.

regulation centers to those places where metabolic processes

When test become larger than 1 cm, this construction is
not the best solution because the chambers become too highoccur (mitochondria, secretory vesicles, lysosomes) or
substances are synthesized (ribosomes, dictyosomes).
In some foraminifera with backwards-bending chambers

and thus fragile (in flat tests).
One solution for test strengthening is fitting the chambers

and division into chamberlets, an additional canal system
is present. It consists of tubes and shortens the productwith tiny pillars.
Another solution is to divide the chambers into smaller,transfer between compartments and the information transfer

equally sized compartments by constructing additionalfrom and to the regulation center (the nucleus). In this casewalls called septula. These small compartments are named

the regulation center is not divided and is typically locatedchamberlets because a chamber is partitioned into smallerin the test center, the first chamber.

－28－

SEM micrograph showing a row of apertures in the lastchamber of Peneroplis (scale bar = 0.1 mm).

SEM micrograph of a broken test of Heterocyclina (scale bar= 0.1 mm) showing openings (stolons) between chamberlets(courtesy by Lukas Hottinger).

arrangement is called annular.
When the annular chamber is divided into chamberlets,
then this series of chamberlets is constructed during a single
growth process, called a cycle. Therefore, such tests arecalled cyclic.
In cyclic tests, a complex system of stolons allows
connections between neighboring chamberlets ofconsecutive growth cycles. In many forms, but not in all
cyclic tests, stolons also connect neighboring chamberlets
SEM micrograph of a broken test of Archaias (scale bar = 0.1mm) showing pillars that strengthen the chambers (photo C. Baal).

of the same growth cycle.
In some foraminiferan architects, the initial test partshows the original construction plan of the planipiraltest, but in many forms, these test parts are simplified bydeveloping initial parts starting with a complex of large
chambers that deviates from the ’normal’ chamber in form

SEM micrograph of the broken test of Heterocyclina (scale bar= 1 mm) with a complete division of chambers into chamberlets
showing the transition from a logarithmic spiral into a cyclicarrangement of chambers (courtesy by Lukas Hottinger).

To reach extreme sizes (more than 1cm) the backbendof chambers also becomes extreme, leading to envelopmentof the whole former test by a single chamber.
Many species exhibit this transition from an initiallyplanspiral arrangement of chambers to a circulararrangement, and the original planispiral construction planis visible in the inner part. When an enveloping chamber
is built during a single growth process, the chamber

X-ray micrograph of Sorites (size = 3.4 mm) showing acomplete cyclic arrangement of chambers subdivided into
chamberlets and an embryonic part ( = nepiont) consisting of aspherical first chamber and a tubular second chamber.

－29－

and size. These complexes are called embryonic apparatus

just below the extremely turbulent reef edge (10 to 30 m

and sometimes nepiont.

depth).

The advantage of a large embryonic apparatus is that the

Depending on the water energy, which the test has tocyclic construction can start with a large size. This lessens

resist, the length/diameter ratio changes. More rounded

the danger that young individuals will be eaten by smaller

forms are abundant in higher energetic regions, while long

predators and enables accelerated growth.

forms are characteristic for less energetic, but still turbulent

Flat and thin tests are ideal for gardeners living inwaters. Nevertheless, all porcellaneous gardeners are

deeper parts of the ocean, where light intensity is low but

restricted by their test ultrastructure to shallow environments.

still enough for the symbiotic algae to photosynthesize.

In clear ocean water, this depth limit is about 60m.

Such tests, especially the cyclic tests, are inappropriate for

Similar to the flat forms, the fusiform growth leads to an

shallow water. There are two reasons for this. First, lightincrease in chamber volume, slowing down the biochemical

intensity is too extreme near the surface: the dangerous UV

and metabolic processes. This calls for a division of theradiation penetrates tropical clear water down to 20 m andlong chambers into smaller chamberlets, and also requires adamages the DNA in the cell nucleus. Second, the strong

system of connections between the neighboring chamberlets

water movement can fracture the construction.

and chamberlets of the succeeding chambers. Since each

Nevertheless, one group of gardeners with cyclic tests
surmounts these difficulties. First, extreme irradiation ischamberlet of the final chamber opens to the outside, these
forms are characterized by a number of apertures.

weakened by the test structure (porcellaneous walls), where

This spindle-shaped construction is the oldest, firstthe extremely tiny and unordered crystals fraction anddeveloped ~300 million years ago, when primitive

partially refract the light. Only a small proportion of theamphibians and the oldest reptiles (long before dinosaurs

light reaches the cyctoplasm and the microalgae. Second,

evolved) lived in woods of ferns and horsetails, the origin

such tests withdraw from the high water energy by usingof black coal.

their pseudopods to attach to flat surfaces like sea grass

We have regarded foraminiferan architects thatleaves or the smooth thalli of larger red and brown algae.

started with an original construction plan as a series of

Smooth and flat rocky bottom are also suitable substrates

chambers that are spirally arranged in a plane. As notedfor cyclic gardeners to attach and escape strong water

above, strepto- and trochospirally coiled tests seem to beenergy.

disadvantageous for constructing large and flat glasshouses,

Smaller foraminifera with porcellaneous tests that

but this is not completely true for trochospiral tests. In

are not endangered by UV light resist water energy bysmaller foraminifers we find extremes in the trochospiralhiding and attaching themselves in the dense network ofform, from extremely high-spirals to a very flat trochospiralfilamentous algae covering the rocky substrate or in smallcoiling, whereby the latter approximates the planispiralgrooves and holes of the reef crest.

coiling.

Gardeners with porcellaneous test walls and tests larger

In trochospiral tests there is a distinction between thethan 5 mm developed yet another strategy of constructing

spiral side and the umbilical side. All whorls are visible on

glasshouses when living in high energetic environments

the spiral side, while only the last whorl can be seen fromwithout the possibility of attaching to smooth and flat

the umbilical sidesurfaces. They use the initial construction plan of a ‘SpiralSome foraminifers became gardeners despite theirof Archimedes’, whereby they maintain the chamber

trochospiral construction. The low trochospiral tests areheight rather constant after an initial increase. Contrarysize-restricted, but can become very thick by enveloping

to the growth mode for becoming flat tests, they elongate

chambers. This yields so-called involute tests, where only

their chambers along the coiling axis. This strategy yields

the last whorl is visible from both sides. These lens-shaped

spindle-shaped, so-called fusiform tests (Figure 6).

tests with a maximum size of 4 mm are appropriate for

These constructions are not adapted to the highest water

living in regions of high, but not extreme water turbulence.

energy and can be found at the edge of a coral reef and on

These forms use pseudopods to attach to the substrate andthe reef crest; gardeners with this type of construction live

resist water turbulence by living in small holes or caves oftoday in holes and grooves at the high energetic reef slope

rocky bottoms－30－

Figure 6. Test constructions in modern larger foraminifera (drawings except Alveolina after Carpenter 1858, Alveolina modified after
Reichel 1936).

－31－

outermost whorl. In this type of construction, in which thechamber wall covers the complete former test during eachchamber construction process, the walls are composed ofmany layers. These are termed lamellae and are especiallyevident in the central part.

The foraminifer Amphistegina lessonii (size = 2.2 mm) with alens-shaped test fixing to algal mat at 0.5 m depth.

Some forms with extreme flat trochospiral coiling
become rather symmetrical with no differences between
the spiral and umbilical side. These truly lens-shaped forms
prefer sandy bottoms, where they live between the grains.
Their lens-shaped tests enable them to easily dig back tothe surface if they become buried by tropical storms, which

The thick lens-shaped foraminifer Amphistegina lobifera (size= 2.1 mm).

shift and suspend the sand.

The foraminifer Amphistegina radiata (size = 3.5 mm) loosely
attached to calcareous grains from 30 m depth.

Axial thin section through the test of Amphistegina lobifera(diameter = 1.8 mm) showing the flat trochospiral enrollment, theporous wall and the large transparent plugs leading light into thetest center (photo E. Iordanova).

Because of this construction and due to the high content
of organic matter between the lamellae, walls are only

These flat trochospiral forms with thick tests protect

transparent at the outermost test part, but become non-themselves against dangerous UV-irradiation by hiding

transparent in the test center. Therefore, such gardeners

in holes and caves. Since the tests are rather small, not all

develop special constructions for getting light into thesymbiotic algae that inhabit the cell plasma of the gardener

innermost whorl. All gardeners living in highly illuminatedcan live in the last whorl. However, only this whorl

areas construct a totally transparent, glassy central test part.

provides enough sunlight for photosynthesis. The space

These so-called plugs are not divided by organic material.

for microplants is thus too small when it is restricted to the－32－

Now, light can penetrate into the inner test and enables

A second way for light gathering is to develop so-called

photosynthesis for the microalgae living in the inner

papillae. Papillae are round, hemispherical elevations atchambers.
Since gardeners also try to live in deeper regions withthe test surface, like pustules, with a glassy, transparent

extreme low light intensities (but enough for photosynthesis

structure. They do not act as lenses to focus light becauseof their microplants), they must provide this weak light forat depths below 50 m light is not directed, but scattered.

their symbionts. The foraminiferans follow two strategies.

Therefore, these papillae reflect the light, which is normallyFirst, the lamellae of the wall became extremely thin whenlost in the water, to the test surface.

covering the former test parts. Since the animal’s volume
does not change as depth increases and the lamellae become
extremely thin, the test diameter also remains the same, but
the test itself becomes very flat.

The flat lens-shaped Amphistegina papillosa (size = 1.2 mm)

The flat lens-shaped Amphistegina bicirculata (size = 1.6 mm)

Axial thin section through the test of Amphistegina papillosa(diameter = 1.1 mm) showing the flat trochospiral enrollment,
the thin porous wall and the numerous papillae for concentrating
dispersed light to the test surface (photo E. Iordanova).

Another group of gardeners prefers to inhabit highly
illuminated regions with extreme water turbulence. They
also originate from ancestors constructing flat trochospiral
Axial thin section through the test of Amphistegina bicirculata(diameter = 1.5 mm) showing the flat trochospiral enrollment andthe thin porous wall (photo E. Iordanova).

tests, but in contrast to the smooth and round tests of theformer group, they construct spines for attach and anchor to
the substrate (Figure 6). These spines, which can be present－33－

in different numbers, forms and lengths, have internal
canals in which the cell plasma flows. Beyond the foramina
in some forms, these spines provide additional connections
to the outside. In a few species lacking foramina, spines
are the only connections between the gardener and its
surrounding.

The globular Baculogypsinoides spinosus (body diameter = 2.5mm) with 3 strong spines.

The thick lens-shaped Calcarina gaudichaudii (body diameter= 1.8 mm).

Axial thin section through the test of Calcarina gaudichaudii(diameter = 1.8 mm) showing the trochospiral enrollment and thethick porous wall (photo E. Iordanova).

To attach to the substrate, the anchoring spines

Axial thin section through the test of Baculogypsinoides
spinosus (diameter = 2.8 mm) showing the trochospiral enrollmentof the central part with thick porous wall and the lateral chamberswith thin walls (photo E. Iordanova).

themselves are additionally equipped with a special glue

Finally, in the most developed architects of this group,that attaches the end of the spines to the substrate. The

the trochospiral arrangement of the main chamber series isadhesion is strong enough to require force to detach theabandoned: a cyclic arrangement is initiated after a shortindividuals.

initial spiral.

For developing spherical glasshouses, which are

Adding lateral chambers at both sides of the main

advantageous in extremely turbulent water, some of thesechamber plane leads to globular, spherical chambers. Only

gardeners, instead of thickening the walls with lamellae, put

the arrangement of spines signalizes the original coiling

additional chambers at the spiral and umbilical test side.

plane.
－34－

makes these tests intransparent, although the walls are

The reproduction of greenhouse gardeners(Figure 3)

hyaline. Thus, only microplants concentrated near the test

The building of a complex embryonic apparatus issurface get enough light for photosynthesis, while the innerpossible only during asexual reproduction. After division,chambers are light depleted. Such test constructions are

every nucleus is surrounded by a portion of the parental

therefore characterized by numerous pillars that are totally

cytoplasm possessing all the organelles necessary for life.

translucent and penetrate the tests down to the center. This

This unit is separated by cell membranes from other nuclei,

enables photosynthesis also for the microalgae living in thethus becoming single individuals. Some microalgae also

inner test parts.

become members of the new daughter cell. This results in

The thick, lamellar walls and abundant organic material

the transfer of the symbiotic plants from the parent to thedaughter individuals.
These embryonic cells with abundant cytoplasm
grow and form the embryonic apparatus by mineralizing
the test wall. Afterwards, they leave the sphere of theparental test and start their independent life. The numberof juveniles leaving the parental organism ranges froma few hundred to more than 2000 individuals in largesized species. All have a good chance to survive and toreproduce. The disadvantage of asexual reproduction is
the spatial restriction: these large benthic forms that crawl
slowly on the sea bottom cannot surmount inconvenientenvironmental conditions such as lowered light intensities(reduced water transparency due to suspended organic andinorganic material during the monsoon season), lowered
temperatures in winter, salinity changes, etc.
To negotiate such environmental barriers and even
The globular Baculogypsina sphaerulata (body diameter = 1.5mm) with strong lateral spines ordered in an equatorial plane.

geographical barriers like the deep ocean bottom between
islands, the second type of reproduction － the sexual
reproduction －　 enables individuals to spread more widely.
Individuals with the single set of genes grow to adultindividuals (gamonts) and reproduce, at the end of theirlives, tiny gametes 20 to 40 micrometers in size. These
gametes possess 2 to 3 locomotion organs, each termed aflagellum. Such gametes are identical in form and are also
known as isogametes. One parental individual releases
ten to one hundred thousand gametes into the water,where they actively swim using the flagella as propulsion.
After conjugation of two gametes, the new individual,
called zygote, is characterized by the double set of genes.

Axial thin section through the test of Baculogypsina
sphaerulata (diameter = 2.3 mm) showing the flat trochospiralenrollment of the first chambers continuing into an equatorial
layer that extends into a spine. Look at the huge number of lateralchambers interrupted by transparent piles extending into the test
center (photo E. Iordanova).

Since the gametes are tiny, the zygote is also extremely
small. The new individuals remain small after growing
to three-chambered individuals with calcified tests. Theirdensity is lower than that of seawater. Thus, they float inseawater (plankton) and can be transported by currents.
This explains the broad distribution of benthic larger
foraminifera, which are restricted to shallow, warm and－35－

clear water environments, over all tropical and subtropicalinsufficient, the host must die.

ocean islands, even though the islands can be separated by

When there is too much light, plant photosynthesis is reduced,

thousands of miles with deep (~4000 m) ocean bottoms,

especially in the case of diatoms, dinoflagellates and red

where the gardeners could never live and survive as full-algae. Green algae, on the other hand, achieve optimum

grown organisms. These individuals with a very small

production rates under strongest light at the surface. At

embryonic part are called agamonts. They grow muchthe water surface, the decrease in the photosynthetic rate

larger compared to the generation with a large embryonicof diatoms is caused by photoinhibition, mainly throughpart, especially in large symbiont-bearing foraminifera.

UV-radiation, which damages the photosynthetic system.
Dinoflagellates have gained the ability to transform thisdangerous short-waved UV-light into harmless wavelengths
by special pigments. Therefore, gardeners living at
the surface and housing diatoms as plants had to build
glasshouses to protect their plants against UV-radiation,
while gardeners housing dinoflagellates can be exposed tostrongest sunlight.
Temperature
Second, gardeners need warm water, which is foundin (warm) temperate to tropical seas. As explained above,

Sexual (small tests) and asexual (large test) generation of
Cycloclypeus (scale bar = 10 mm; photo C. Baal).

temperature is important for the availability of hydrogencarbonate and carbonate ions during the calcification
process of the test. Larger foraminifera can survive

The settlement of greenhouse gardeners

temperatures below the minimum survival temperatures

What are the conditions for those larger foraminifera(MinST) up to a few (maximum 2) weeks. The minimum
survival temperatures differ between gardeners, but neverthat act as gardeners and that construct greenhouses?

fall below 14℃. In species restricted to shallow tropicalLightseas, these minimum survival temperatures are about 19℃.

First, gardeners have to live in illuminated water

Nothing is known about maximum survival

down to those depths where their cultivated plants, thetemperatures (MaxST) of gardeners. Here we have to

microalgae, can still get a ‘positive net production’. A

differentiate between the MaxST of the gardener and thepositive net production means that the carbon produced by

MaxST of the plants, which can strongly differ. Lengthierphotosynthesis (main elements of sugars and fats) exceeds

temperature increases higher than the MaxST of the micro-

the carbon (carbon dioxide) lost by respiration by the algae.

algae block photosynthesis and build up products that

The depth at which the rate of respiration is equal to thepoison the algae. In such cases, for example when corals

rate of photosynthesis is called the compensation depth.

act as hosts, they can spit out the symbiotic algae (naked

Compensation depths differ between the microalgal groups

dinoflagellates known as zooxanthellae) and becomeused by foraminifera and depend on water transparency. In

uncolored. This is the well-known ‘coral bleaching’ thatclear water, such as in the tropical and subtropical ocean far

has damaged coral reefs in the late 1990s. Bleaching is also

away from large land masses or in desert (arid) zones, red

found in larger foraminifera, but raised temperatures arealgae are characterized by compensation depths more than

not the cause. In some foraminifera, high solar irradiation

300 m, followed by diatoms (~200 m) and dinoflagellatescaused by ozone depletion damages the plants, which in this(~150 m), while green algae are restricted to shallower

case are diatoms. Contrary to coral polyps, the foraminifer

regions (~80 m). When microalgae are unable to get adigests all damaged diatoms and becomes partially

positive net rate sufficient for the host’s metabolism, thenbleached.

the host digests the plants to obtain food. Afterwards, if no

Normally, foraminifera can survive high temperatures

food becomes available or the uptake from the outside is(~45℃), especially species with porcellaneous walls.

－36－

Therefore, the cultivated plants ultimately define the upper
temperature limit of the gardener.
Footing
It is important for all gardeners to move theirglasshouses into the best position for light. This can bedone, on the one hand, by climbing to sunlit places togather more light or, on the other hand, by hiding in small
holes, caves or beneath larger plant leaves, algal thalli(constructed similar to leaves in larger algae) or rubble toreduce irradiation. Therefore, the substrate for footing ofglasshouses differs. It can be organic material like algal
thalli and algal rhizomes (whose function is similar to roots

Meadows of the sea grass Enhalus (leaf length =1,200 to 1,500mm) in the shallow lagoon at Peleliu, Belau.

in land plants but is restricted to attachment to the bottom).
Gardeners avoid living on animal tissue like coral polyps orsponges. Some gardeners rest their tests on rocks, boulders
and coarse sand; a very few prefer fine-grained sediments
like fine sand and silt.
Since water movement by waves and currents is
responsible for the development of sediments and also
determines the distribution of larger plants, the gardeners
have to resist being swept away (entrainment) from thesurface by fixing mechanisms in turbulent water.
Let’s have a look at some footing possibilities:
a．Flat and smooth surfaces as found on seagrass leaves orlarge, smooth algal thalli are inhabited by flat, disc-shaped
gardeners.
In that case, the biconcave tests hinder entrainment fromThe foraminifer Amphisorus (size = 40 mm) attached to thesmooth surface of the sea grass Enhalus.

the surface by creating negative pressure at the test sideoriented to the leaf surface. Additionally, these gardeners

b．In the uppermost meters of the sea, light-oriented

fix their tests with gluey pseudopods. These extrude fromrock surfaces and boulder are densely overgrown by

the numerous apertures at the test periphery and are used tosmall, filamentous macroalgae possessing thalli of a few

feed on extremely small microorganisms like bacteria andmicroalgae living on the surface of leaves or thalli.

Shallow lagoon at Peleliu, Belau. The open sea is behind thereef crest right in the background.

Fringing reef in front of a rocky coast (Cape Bise, Motobu,
Okinawa) during tidal low stand showing the clear zonation fromthe coast to the reef moat, always covered by water, and to the reef
crest that is falling dry during low stand. The waves of the open sea
are braking at the reef crown.

－37－Fringing reef in front of a sandy coast NW of Kabira Bay,
Ishigaki, Okinawa, Japan showing the transition from the sandy
beach to the broad reef moat.

millimeters length. Sand grains from 100 micrometer to 1

Sand grains caught by fine filamentous red algae, where
foraminifera of the genus Peneroplis with symbiotic red microalgae are protecting against light and waves (scale bar = 1 mm).

mm in size are trapped within this algal turf. Lens-shaped

tips of the spines has a strong glue that fixes the glasshouseflat foraminifers settle between the grains, attaching withto the algae. Water movement alone cannot entrain

pseudopods extruding from the multiple apertures to thethese gardeners from the algae. Here, forceps or strong

rocky bottom or algal filaments.

mechanical force is required to separate the foraminifer

With this life style, these foraminifera resist entrainment

from the algal thallus.
d．The bottom side of boulders deposited in the uppermost

under highest water motion and energy.
When these surfaces are more or less flat, thenmeters lacks algal cover; gardeners that are not adapted toalso larger gardeners with flat, disc-shaped biconcave

extreme irradiation can hide at such more or less weakly

glasshouses can settle, again attaching with gluey

illuminated places.
Small gardeners with thick, lens-shaped glasshouses

pseudopods to the filamentous algal turf.
c．Larger macroalgae with sizes up to 10cm that have alive beneath boulders, using tiny holes as hideaways to

network of filamentous to rod-like thalli can be found atresist entrainment by water movement. They weakly attachsites with extreme water energy. Gardeners living withinto the boulders by pseudopods extruding from a single

these dense networks are distinguished by lens-shaped

small aperture, and can therefore be more easily entrained.

glasshouses having long, thick spines, giving them theAdditionally, they cannot block irradiation like the above-

appearance of little stars or sun discs.

described gardeners living in extremely illuminated regions.

These spines act as anchors within the thalli or between

This explains life at energy- and light-protected sites.

the glasshouses, whereby cyctoplasm extruding from theIn the uppermost part of coral reefs that face the open

Shallow reef moat north of Sesoko Island, Okinawa, Japan. The
rocky bottom is partly covered with sand, where a few stony corals
are living. The filamentous red algae Jania covers the bottom,
where sea cucumbers and sea urchins are living.

Boulder of the reef moat close to the reef crown with filamentsof the green algae Halimeda (scale bar = 15 mm), densely settled
by large Amphisorus and small Peneroplis.

－38－

Reef moat close to the crest at Kabira Bay, Ishigaki Island,
Japan showing the dense settlement of the foraminifer Amphisorus
on coral rubble (scale bar = 100 mm).

Living sand on the reef crest of Hateruma Island, Japan (scalebar = 10 mm).

Reef crest NW of Kabira bay at tidal low stand, which isdensely covered by filamentous red algae mixed with green algae.

Foraminiferal fauna from the reef crest with the star shaped
Calcarina calcar, Calcarina gaudichaudii and Baculogypsina
sphaerulata, the thick lens-shaped Amphistegina lobifera an the
purple Peneroplis antillarum (scale bar = 1 mm)

Living foraminifera of genera Calcarina, Baculogypsina andPeneroplis in the dense meshwork of filamentous red algae fromthe reef crest (scale bar = 10 mm).

sea, the rocky surfaces are overgrown by red algal crusts(corallinacean algae). These algae are preferred places forlarger foraminifera, especially when these rocks are wellstructured with small holes and caves, where the lensand cigar-shaped gardeners can best resist the high waterenergy.

Reef crown of the fringing reef NW of Sesoko Island, Okinawa,
Japan consisting mainly of the tabular stony coral Acropora
resisting extreme water energy.

－39－algae, fractured shells of clams and snails and spines of sea
urchins. Therefore, the size of the grains is similar to that of
the gardeners. When the slope in front of the reef is gentle,
the proportion of sand increases with depth, and the sandbecomes finer.

A 2 m deep groove in the reef crown caused by strong rip
currents (speed ~ 2 meters per second) flowing seawards from thesurf zone where waves are braking.

e．In areas of the upper reef slope that are protected fromstrong wave action, sand with large grain size (1-2 mm)
is mixed with gravel (> 2 mm). Most sand- and gravelsized particles are broken coral pieces and corallinacean

The spindle shaped foraminifer Alveolinella (size = 2.5 mm)
attached to coral cobble.

Bottom of the groove covered by large boulders of broken
corals and rocks.

Surface of a boulder, which is totally covered by calcareous
corallinaecean red algae. Thick lens shaped foraminifera of thegenus Amphistegina are hiding in small holes (scale bar = 1 mm)

Sandy bottom at 5 m depth on the reef slope north of Sesoko
Island, Okinawa, Japan. This sand is deposited in quiet regions of
the slope.

－40－

Rocky bottom at 30 m depth north of Sesoko Island, Okinawa,
Japan, which is the base of the coral reef (distance between stripes= 10 cm; photo F. Tatzreiter).

Foraminiferal fauna from the upper reef slope with the star
shaped Calcarina hispida, the spindle shaped Alveolinella quoyi,
the lens-shaped Amphistegina radiata and the flat disc-shaped
Amphisorus hemprichii (brown) and Parasorites orbitolitoides(green) (scale bar = 10 mm).

The gardeners live on or in the substrate. In the latter
case, they use the space between grains, but do not dig too
deep into the sand so that they still attain enough light.
These glasshouses are always thick lens-shaped. This form
makes it easier to climb up to the surface if they becomeburied by sediment transported by storms.
f．As explained above, the sand becomes finer withincreasing depth. Therefore, the grain size of the sedimentnear the compensation depth in clear ocean water isbetween 0.063 and 0.25 mm. This sediment type is called’fine sand’. In this case the sand grains are much smaller
Living Operculina (size = 3 mm) burrowing in coarse sand of
the fore reef area

than the glasshouses of the gardeners. In contrast to sandgrains, which become smaller with increasing depth, theglasshouses become larger with depth in order to gather
enough light for their micro-plants. The largest glasshouses
with transparent (hyaline) test walls are found here. Today
they reach sizes of a few centimeters!

Typical bottom sediment of the upper reef slope at 40 m depthwith the living foraminifera Heterostegina and Amphistegina (scalebar = 1 mm)

Sandy bottom at 50 m depth northwest of Sesoko Island,
Okinawa, Japan, that is covered with larger particles, so-called
macroids (distance between stripes = 10 cm; photo F. Tatzreiter).

－41－

allows the foraminifera to get the best position in or on thesediment; therefore, lens-shaped tests are advantageous.

Foraminiferal fauna from the deeper reef slope with the lensshaped Amphistegina radiata, the star-shaped Baculogypsinoides
spinosus and Calcarina mayori, and the flat large planspirally
coiled Operculina complanata and Heterostegina depressa (scalebar = 10 mm).
The thick lens-shaped Operculina discoidalis (size = 2.5 mm)
living on muddy bottom at 18 m depth in the lagoon west off
Motobu town, Okinawa, Japan.

The clans of gardeners
According to their genetic relationships, which
are proven by very complex molecular techniques, we
distinguish seven clans of gardeners today. In zoologicalsystematics these clans are called families. Besides
molecular relationships, the attribution of a gardener to
The disc-shaped Cyclocyleus carpenteri (diameter = 15 mm)
living at 70 m on sandy bottom.

a clan is supported by wall mineralogy and structure,
glasshouse construction, and specification of their cultivatedplants, the microalgae.

All gardeners with large, flat tests live on the bottom
surface, not in the sediment (where they would be unable

Purple gardeners, scientific name Peneroplidae

to get enough light for their plants). The flat and large

This clan of gardeners cultivates single-celled red

tests have the advantage that, after becoming suspended

algae (Porphyridium). Living individuals are therefore

by tropical storms, which affect sediments down to 150 m

characterized by an intensive purple color caused by thesewater depth, the smaller sand particles settle earlier than theplants.

plate-like glasshouse after the waning storm. This reduces

Empty tests are smooth and white, like porcellaneous

the threat of becoming buried in the sediment: the gardeners

coffee cups. This is caused by the total reflection of light.

do not have to dig to the sediment surface, which is difficult

The transparency of walls necessary for light penetration isfor forms possessing large and flat tests.

obtained by pits that are arranged in straight grooves.

g．Sediment finer than 0.063 millimeter is called silt or

The construction plan starts with a spherical first

mud. These sediments can be found only in the deeper parts

chamber and a short tubular second chamber. The followingof gently inclining slopes facing the open sea, much deeper

chambers are arranged in a spiral plane. Chamber height isthan the compensation depth, or in protected areas likerelatively small and does not increase during growth, whilelagoons. In the first case, no gardeners live at these depths

chamber width strongly increases in some representatives.

because of insufficient light. Gardeners living in lagoons

Enrollment of the spiral can be weakened in younger tests,

on or in an extremely fine silt or mud are characterized

resulting in a straight chamber arrangement.

by lens-shaped tests, similar to the forms found on or in

Test openings are irregular in outline and often tree-coarse-grained sand. Here, the ability to dig is important: it

shaped (dendritic) in thick forms, becoming a series of－42－

SEM micrograph of the test surface of Peneroplis pertusus
showing pseudopores within the striae (scale bar = 0.01 mm).

SEM micrograph of the test surface of Dendritina zhengae
showing pseudopores on the smooth test surface, that do not
penetrate the wall (scale bar = 0.01 mm).

rounded openings in flat forms. This promotes spreading

SEM micrograph showing an irregular opening (aperture) at theend of the final chamber of Dendritina ambigua (scale bar = 0.1mm) remembering a tree (dendros), therefore the name dendritic
aperture and the name Dendritina.

SEM micrograph showing a row of round openings bordered
by a rim at the final chamber of Peneroplis planatus (scale bar =0.1 mm).

of pseudopods and clinging to the substrate, preventing
In a third group of purple gardeners, both chamber

entrainment by strong water movement like waves andheight and width slowly increase with growth: after a short

breakers.
The normal size of ‘adult’ individuals is between 1 andspiral initial part, the chambers are arranged in a linear
series and lose contact with the initial spiral part (Peneroplis

2 mm; a few can grow up to 3 mm.
Clan members divide the habitat according to theirpertusus). Robust tests with this chamber arrangement are

different requirements (habitat partitioning). Flat forms, inrare in energy-dominated regions of the upper breaker zone,

which chambers keep contact with the spiral part even in

becoming more abundant in protected deeper parts down tostraight tests, prefer shallow water and prevent entrainment

40 m depth, preferring rocky bottoms.

by strong breakers by hiding between and clinging to small

Small and fragile forms are extremely rare and prefer tofilamentous macroalgae covering the reef crest in tropicalsettle in the most protected parts of the uppermost regions.

seas (Peneroplis antillarum, Peneroplis planatus).

They would be completely destroyed and fractioned in

Gardeners with thick lens-shaped tests avoid extremely

regions with permanently moving sediment like sands.

shallow water because they cannot resist strong water

Purple gardeners are not restricted to tropical seas,energy (Dendritina). They prefer clear ocean water in thebut can also be found in warm temperate oceans, where

uppermost region from 10 to 40 m depth, where they live

winter temperatures sink below 14℃. Their geographicalbetween sand grains. They cannot be found on steep reef

distribution is worldwide, whereby their presenceslopes because sandy sediments are transported to deeper

throughout the Mediterranean is remarkable.

regions, where peneroplids cannot survive.
－43－

Living Dendritina ambigua colored by purple microalgae(scale bar = 1 mm).

Living Peneroplis antillarum colored by purple microalgae(scale bar = 1 mm).

SEM micrograph of Dendritina ambigua (size = 1.2 mm).

SEM micrograph of Peneroplis antillarum (size = 1.2 mm).

SEM micrograph of Peneroplis planatus (size = 1.8 mm).

SEM micrograph of Dendritina zhengae (size = 1.4 mm)
possessing a smooth porcellaneous shell.

－44－

a distinct double row with alternating apertures after an
initial single row stage.
Members of this clan show greater variability in theirconstruction plan and size compared to purple gardeners.
The simplest constructions are similar to purple gardeners,
showing the same planispiral coiling, where chamber heightremains constant (Laevipeneroplis). The chambers always
keep contact with the initial spiral, surrounding the former
test when the chamber arrangement becomes straight. In
contrast to purple gardeners, tests are smooth, and light
penetrates the thick walls through pore-like structures.
These structures do not penetrate the thick walls but makethem thinner in places.
Clan members showing the initial test construction
explained above can grow to more than 3 mm. In large
individuals, chambers envelop parts of the older test.

SEM micrograph of Peneroplis pertusus (size = 1 mm)
showing a weak increase in chamber height and evolute coiling,which means that the inner whorls are visible from outside.

SEM micrograph of Peneroplis pertusus with final chambersthat are arranged in a straight order (size = 1.4 mm).

SEM micrograph showing the row of round openings bordered
by a rim at the final chamber of Laevipeneroplis proteus (scale bar= 0.1 mm).

Green gardeners, scientific name Archaiasinidae
Similar to purple gardeners, the clan members possess
white and non-transparent porcellaneous walls. The
intensive green color is caused by their symbiotic plants,
which are green algae (Chlamydomonas). In contrast
to purple gardeners, where the openings (aperture) areelongate, oval or irregularly dendritic, these greenhouses
always show a series of regular circular to oval openings
surrounded by a small rim. Most of these openings become

SEM micrograph showing the row of round openings bordered
by a rim at the final chamber of large Laevipeneroplis proteus(scale bar = 0.1 mm).

－45－

SEM micrograph showing the double row of roundopenings bordered by a rim at the final chamber of verly large
Laevipeneroplis proteus (scale bar = 0.1 mm).

These gardeners are restricted to shallow waterwith weak water movement, for example in waveprotected shallow reef and backreef areas (reef moat)

SEM micrograph of Laevipeneroplis proteus (size = 0.6 mm).

in the Caribbean, where they are abundant. A very few
representatives can be found in the central tropical West
Pacific.
Similar constructions with large flaring chambers areabundant in protected areas of the shallow sea, attaining
sizes of up to 4mm. Due to the larger size they haveto strengthen their tests with pillars, which divide thechambers into smaller units; a complete separation by
septulae, however, is not attained.
Much larger and thicker individuals with lens-shaped
tests densely settle on macroalgae of the high-energy reef
flats in the Caribbean (Archaias). They also strengthen
their constructions with pillars, and the strong backbend ofchambers is characteristic.
Sea grass meadows of deeper water down to 10 m
depth are inhabited in the Caribbean by flat circular tests
SEM micrograph of Laevipeneroplis proteus with chambers
embarrassing the former test part (size = 1.2 mm).

with a thicker initial part similar to their back reef relatives(Cyclorbiculina). The chamber envelopment visible in therelative is completed in these forms. This leads to ring-like(annular) chambers that are divided by pillars. Size often
exceed 1 cm.
A quite different construction plan characterizes thelast clan member (Parasorites). Test construction starts
with a flat initial spiral quite similar to flat purple gardeners(Peneroplis planatus ), immediately transforming into ringLiving Laevipeneroplis proteus (size = 2.1 mm) on sandy
bottom in the shallow lagoon of Peleliu, Belau.

like annular chambers. The distinguishing feature from thethree above-described relatives is the complete division of－46－

SEM micrograph of Cyclorbiculina compressa with chambers
partly embarrassing the former test part (size = 1.6 mm; photo C.
Baal).

SEM micrograph of Archaias angulatus with chambers
embarrassing the former test part (size = 1.5 mm; photo C. Baal).

Light micrograph of Cyclorbiculina compressa (size = 2.4 mm)with chambers totally embarrassing the former test part (photo C.
Baal).
SEM micrograph of the oval, rimmed openings of Archaias
angulatus in the final chamber (scale bar = 0.1 mm; photo C. Baal).

the chambers into chamberlets that are separated by walls
called septulae. Additionally, the inner part is not thickened
like in other clan members with flaring chambers.
Membership in the clan of green gardeners is alsocharacterized by equally sized pores surrounded by small
rims that are arranged in a single row; this leads to double
rows in larger (up to 1 cm) tests. The last group again isabundant in the Caribbean, but can also be found in thetropical West Pacific, where it settles in clear ocean waterfrom 30 to 60m. This is extremely deep for gardeners
with porcellaneous tests because light is weak at thosedepths and lacks the red wavelengths that are necessary for

Light micrograph of living Parasorites orbitolitoides (size =2.3 mm).

photosynthesis of green plants.
－47－

This makes the colors in the soritids also highly variable,
differing and changing from place to place.
Three main types live in the shallow tropical and warm
temperate oceans. The first group (Sorites) constructs flatglass houses with a single row of openings.
They live attached to flat and firm substrates like sea
grass leaves, larger thalli of macroalgae or on smooth rocky
bottom. Especially in the latter case, they adjust their test
according to the form of the substrate. Abundance is highest

SEM micrograph of the lateral side of Parasorites orbitolitoides
showing a single row of oval openings without a rim (scale bar =0.01 mm; photo C. Baal)).

Blue to brownish-violet gardeners, scientific name
Soritidae
These gardeners are characterized by large, circular
test constructions attaining sizes of up to 3 cm. Walls are
porcellaneous and transparency is obtained by an extreme
thinning of the wall, which acts like the window panes inglasshouses. Therefore, their test construction is the mostsimilar to glasshouses constructed by human engineers.
The large initial chamber is followed by a tubular second

SEM micrograph of Sorites orbiculus (size = 1.5 mm).

chamber, which is then immediately surrounded by rings ofchambers with glassy windows.
The bluish to brownish-violet color originates fromthe microalgae, which are dinoflagellates as in corals. In
corals, most of the different colors are caused by symbionts.

Thin section of Sorites orbiculus showing the transparent testparts at the chamber surface (size = 1.3 mm; photo E. Iordanova).

Living Sorites orbiculus (size = 1.4 mm) fixed to a coral
boulder.

SEM micrograph of the lateral side of Sorites orbiculus
showing a single row of inclined apertures consisting of the
openings of contiguous chambers (scale bar = 0.01 mm).

－48－

at the surface in quiet waters, living attached to sea grass,but they can survive in clear water down to 50 m depth.
The geographical distribution, similar to purple
gardeners, is not restricted to tropical seas but also ranges
to warm temperate regions. The northern distribution limits
are Florida in the West Atlantic, Sicily in the Mediterraneanand Kii Peninsula of Japan in the West Pacific.
The second group belonging to this clan (Amphisorus)
shows a construction plan similar to the first group. It
differs somewhat in that it becomes larger and thicker
by alternating chamberlets, causing increasing thickness
during test growth. Therefore, test openings are arranged ina double row.
The shallow-living forms become thicker compared tothe deeper-living forms. Thus, a median layer of irregularopenings is positioned between the two main rows.

SEM micrograph of Amphisorus hemprichii (size = 3 mm).

These gardeners can attain extreme abundances inthe shallowest region of protected reef areas, where they
settle on firm substrate, i.e. attached to the rocky bottom
or fixed to small filamentous algae. In lagoonal areas they
are extremely common on sea grass leaves or on smoothand flat macroalgal thalli. Abundance decreases with depth,
where they can live in clear water down to 50 m. From 5 to
50 m, tests are always thin and do not show intermediate
layers of apertures.
The geographical distribution is more restrictedcompared to its smaller relative. These gardeners are rare in
the Atlantic but abundant in the Red Sea, Indian Ocean andCentral and West-Pacific as far south as New Guinea.
In the Central and SW Pacific a related group withsimilar test form and size replaces the above gardeners

SEM micrograph of the lateral side of Amphisorus hemprichii
showing a double row of drop shaped apertures, alternating due tothe contiguous chambers (scale bar = 0.01 mm).

SEM micrograph of the lateral side of a thick Amphisorus
hemprichii showing a double row of drop shaped apertures with anadditional median layer of double rows (scale bar = 0.1 mm).
Living Amphisorus hemprichii (size = 2 mm).

－49－

SEM micrograph of the lateral side of an extreme thickAmphisorus hemprichii showing the double row of drop shaped
apertures with an additional median layer of several rows ofirregularly formed openings (scale bar = 0.1 mm).

SEM micrograph of the lateral side of Marginopora vertebralis
showing the double row of rimmed and rounded apertures withmedian rows of rimmed circular openings (scale bar = 0.1 mm).

(Marginopora). Beside chamber construction, the mainchamberlet possesses an aperture, becoming the foramendifferences lie in the openings, which are always circular

as a connection to the chamberlet of the next chamber.

and of the same size, surrounded by a rim and arranged in

Moreover, the row of chamberlets within one chamber ismultiple rows.

connected by a specific system of openings, called canals.

The depth distribution of these gardeners is more

These canals are openings in the septula running in front

restricted compared to its close relative, and they can live inof, behind the main chamber wall (septum) or in bothshallow regions down to 10 m.

directions.
Because the walls are porcellaneous, these gardeners

Ocher gardeners with spindle-shaped greenhouses,

have to make their walls extremely thin in the center ofscientific name Alveolinidae

the chamberlet to provide transparency for the symbiotic

These gardeners construct special glasshouses that
resemble a spindle. The form and size of the spindle arevariable, ranging from approximately globular constructions
to very elongate, needle-shaped forms.
The size also ranges from 2 mm in ‘adult’ globular
individuals to 4 cm in the needle shaped forms.
The elongated chambers are planispirally arranged
and subdivided by septula into chamberlets. Every

Living Alveolinella quoyi (size = 3.8 mm).

SEM micrograph of Alveolinella quoyi (size = 4.1 mm).

Living Marginopora vertebralis (size = 3 mm).

－50－

SEM micrograph of Alveolinella quoyi showing themultiplication of rows of rimmed apertures at the spindle edge
(scale bar = 0.1 mm).

SEM micrograph of Alveolinella quoyi showing the grooves atthe shell surface enabling light penetration (scale bar = 0.1 mm).

plants, which are diatoms. Housing diatoms as symbionts
is unique for the gardeners with porcellaneous walls, while
diatoms are the only plants that gardeners with hyaline test
can house. Again, transparent wall regions above every
chamberlet are called ‘windows’. When the gardener isfully active and undisturbed, it attaches the glasshouse to
the bottom with pseudopods extruding from one end of thespindle. The cytoplasm of the host transports the microalgae
into the last whorl to attain enough light for photosynthesis(because photosysnthesis is hampered in the inner whorl).
These gardeners do not live in regions with extreme
water motion at the reef crest, but also do not prefer quiet

Thin section through the spindle shaped Alveolinella quoyi(size = 3 mm; photo E. Iordanova)

shallow water such as is found in the reef moat and inlagoons. They need some water motion, but do not depend
on substrate. In regions with higher water motion, e.g. on
the upper reef slope, they live in small holes of boulders
and reef rock. With decreasing motion they can also live onmobile, coarse sand that is more abundant in deeper regionsof the upper slope. Nevertheless, these gardeners needhighly transparent water, and the deepest-living gardeners
are found in these waters at 50 m depth.
These gardeners with spindle-shaped glasshouses are

Light micrograph of Borelis melo (size = 1.3 mm; photo C.
Baal)

today not represented in the tropical Atlantic. Globular tests
and thick spindles (Borelis ) are found in the Indian Ocean
and the Red Sea, while the long spindle types (Alveolinella )are restricted to the tropical West Pacific.
Olive-green gardeners constructing lentil-shaped
greenhouses, scientific name Amphisteginidae
These gardeners construct small glasshouses between
1.5 and 4 mm, where the chambers are enrolled similar to

SEM micrograph of Borelis melo (size = 1.4 mm) showing thesingle row of rimmed apertures (photo C. Baal).

－51－

a snail shell (trochospiral). But these spirals are extremely
flat, approximating enrollment in a plane. Only chambers of
the last whorl are visible from both sides, making the tests
looks like small lentils. On the lower side (scientifically
named umbilical side) the chamber is partitioned by aseptum-like structure. Therefore, the central part of thelower side of the glasshouses looks like small swastikas.
The amphisteginids harboring diatoms as greenhouseplants develop modifications of the initial construction
plan. This enables them to live in extremely illuminatedenvironments on the one side, but also in light-depleted
environments on the other. Thick glasshouses (Amphistegina
lobifera) are constructed in shallow regions with high, but
not extreme water motion. Here, the amphisteginids fix theirglasshouses to filamentous algae or seek protected areas
in small holes of boulders or in the reef rock. To provide
the microalgae living in the inner whorls of the glasshousewith enough light, these thick constructions show a totallytransparent center, which are known as plugs.
Gardeners with completely symmetrical lentil-shaped
glasshouses (Amphistegina radiata) inhabit shallow ocean
regions with high, but not extreme water motion, wherecoarse sand covers the sea floor. It is difficult to differentiate
between the upper and lower side. The glasshouse openings
are also located at the lateral side and are not adapted for
attachment to firm substrate.
The two groups of gardeners within the Amphisteginidae
react to weaker light at deeper regions in different ways.
The first-mentioned group (Amphistegina lessonii) makes

Living Amphistegina lessoni (size = 1.1 mm), view from thespiral side (upper) with lobate chamber partitions and from theumbilical side (lower) with septal partitions.

very flat tests without changing size (Amphistegina
bicirculata). Thus they are restricted to highly transparent
water to 90 m depth.
The second group with completely symmetrical test also
becomes flatter, but in deeper regions they construct glassy
structures on their surface called papillae to concentrate
the reflected light (Amphistegina papillosa). With thismechanism, gardeners can provide their microalgaewith enough light for photosynthesis down to 120 m intransparent ocean water.
While members of the first group show a worldwide
distribution, tolerating the lowest temperatures of all
greenhouse gardeners and thus extending to the warm
temperate zone, the second group is restricted to the tropicalIndo-Pacific.
Amphistegina lobifera (size = 2 mm) living in shallowest water
showing lobate chamber partitions.

－52－

Living Amphistegina radiata (size = 1.7 mm), view from thespiral side (upper) and from the umbilical side (lower).

Living Amphistegina bicirculata (size = 1.3 mm); view fromthe spiral side (upper) and from the umbilical side (lower), thelatter demonstrating additional partitions by septa.

Ocher gardeners with star-shaped greenhouses, scientificname Calcarinidae
The calcarinids cultivating diatoms construct
glasshouses similar to the former group, with the chamberarrangement in a flat trochospiral and thick walls. The maindifference to the former clan is the construction of longThin section of Amphistegina radiata (size = 2.2 mm; photo E.
Iordanova).

spines, giving glasshouses the appearance of little stars or
sun discs. Spines act as anchors for fixing the glasshouses
to the substrate. Glasshouse size ranges from 2 to 5 mm.
Based on this construction, calcarinids often settle in highabundance in regions with extreme water motion. They－53－

therefore populate the reef crest, where they densely cover
the bottom. Their size, which is similar to coarse sandgrains, and their extreme density, which can be 600,000 per
m2, gives the impression of a sandy floor on the reef flat,but all these sand grains are alive!
Therefore, they are called ’living sand’ or ’star sand’and often sold as souvenirs filled in small glass-bottles.
The calcarinid gardeners construct different types ofglasshouses for settling in shallow regions of the tropicalocean. They need clear ocean water and thus avoid regionswith high fluvial input of fine sediment from the land or
polluted water. This makes them good indicators for healthy
regions of the shallowest tropical seas in the East Indianand West Pacific Ocean.
Calcarinids that construct flat trochospiral glasshouses
where all chambers are visible, and that possess short spines
at the lateral chamber part, are found in the whole tropicalIndian Ocean and West Pacific, where they settle in shallow
regions with little water motion (Calcarina calcar).
All other calcarinids are restricted to the IndonesianArchipelago and the tropical West and Central Pacific
Calcarinids similar to the former group, where theglasshouses have longer spines that are sometimes furcated,

Living Amphistegina papillosa (size = 0.9 mm), view from thespiral side (upper) and from the umbilical side (lower).

“Living sand” on the reef crest of Hateruma Island, Okinawa,
Japan (scale bar = 10 mm).

SEM micrograph of Amphistegina papillosa (size = 0.7 mm).

Small glass bottles filled with “Star Sand”. Souvenir from
Motobu, Okinawa.

－54－

Living Calcarina calcar (size = 1.4 mm); view from the spiralside (upper) and from the umbilical side (lower).

settle in regions similar to the former group (Calcarina
defrancii). Thus they are found in front of or behind theSEM micrograph of Calcarina calcar (size = 1.5 mm); view
from the spiral side (upper) and from the umbilical side (lower).

most extremely turbulent reef crest, clinging to filamentous
macroalgae.
Robust and large glasshouses with a few but very strong
spines resemble little sun disks (Calcarina gaudichaudii).
They lack an aperture, and connections to the environment
can thus only be found at the tips of spines. These gardeners
can resist extreme water motion by clinging to filamentous
macroalgae or anchoring together. This makes them one of
the main members of the ‘star sand’ living in the highest
energetic zone of a Pacific coral reef.
Some gardeners within the calcarinids additionallycover their tests surfaces with spikes that are smaller thanspines. Three types of glasshouses are described, which
depend on water motion. Glasshouses with short spines
similar in length to the long spikes (giving the impression

SEM micrograph of a spine of Calcarina calcar (scale bar =0.1 mm).

of small sea urchins) are found in the shallowest zone, but－55－

SEM micrograph of Calcarina defrancii (body size without
spines = 1.2 mm); view from the spiral side (upper) and from theumbilical side (lower).
Living Calcarina defrancii (size = 1.8 mm); view from thespiral side (upper) and from the umbilical side (lower).

not on the reef crest (Calcarina quoyi).
In upper regions of the reef slope down to 30 m,
calcarinids with longer and robust spines are abundant(Calcarina hispida), while between 20 and 60 m a thirdgroup with long, sometimes bifurcated spines is found(Calcarina mayori).
The last group of gardeners with additional spikes
covering the glasshouse adds additional chambers on
the upper (spiral) and lower (umbilical) side of the mainchamber spiral (Baculogypsinoides). The number of spines,

SEM micrograph of a spine of Calcarina defrancii (scale bar =0.1 mm).

again found as chamber extensions, is reduced to 3. This

Large pustules, similar to plugs in amphisteginids asconstruction results in approximately globular glasshouses,

completely transparent structures, transmit light into theyielding the largest size (5 mm) within the calcarinids.

central test part and thus provide the microalgae living in－56－

Living Calcarina gaudichaudii (size = 2.1 mm); view from thespiral side (upper) and from the umbilical side (lower).

SEM micrograph of the surface of Calcarina gaudichaudii
showing the protection of pores by small spikes (scale bar = 0.1mm).

SEM micrograph of Calcarina gaudichaudii (body size without
spines = 1.2 mm); view from the spiral side and from the umbilicalside.

SEM micrograph of a spine of Calcarina gaudichaudii (scalebar = 0.1 mm).

－57－

SEM micrograph of Calcarina quoyi (size = 1.5 mm); view
from the umbilical side.

SEM micrograph of the surface of Calcarina quoyi showing
the protection of pores by small spikes (scale bar = 0.1 mm).

Living Calcarina hispida (size = 2.5 mm); view from the spiralside (upper) and from the umbilical side (lower).

SEM micrograph of a spine of Calcarina quoyi (scale bar = 0.1
mm).

－58－

SEM micrograph of Calcarina mayori (body size without
spines = 1 mm)

SEM micrograph of Calcarina hispida; view from the spiralside (body size without spines = 1.6 mm) and from the umbilicalside (body size without spines = 1.5 mm).

SEM micrograph of a spine and shell surface of Calcarina
mayori (scale bar = 0.1 mm).

the test center with necessary light.
These gardeners are the only clan members that range
into the deeper regions of the well-illuminated reef slope
between 30 and 60 m.
The last two groups of gardeners within the calcarinids
construct special glasshouses that deviate from the main
trend in calcarinids. The first group (Baculogypsina)
arranges their chambers, after developing a flat and shortspiral, in circular manner around this embryonic spiral.
Four to seven spines are developed at the lateral side of thisplane. Additional chambers are built at both sides of thisSEM micrograph of a spine of Calcarina hispida (scale bar =0.1 mm).

median plane, resulting in thick lens-shaped glasshouses
with strong spines. Totally glassy pustules allow light to－59－

SEM micrograph of a spine and shell surface of
Baculogypsinoides spinosus (scale bar = 0.1 mm).

Living Baculogypsinoides spinosus (size = 3 mm).

SEM micrograph of a spine of Baculogypsinoides spinosus(scale bar = 0.1 mm).

penetrate into the central test part. This construction has
the appearance of little stars and makes this group the main
components of star-sand in the tropical West-Pacific, where
it inhabits regions of extreme water motion.
The last and most developed group within the calcarinid
gardeners constructs glasshouses similar to the former
SEM micrograph of Baculogypsinoides spinosus (body size
without spines = 2 mm).

group with dominating lateral chambers (Schlumbergerella).
The lack of a planispiral initial chamber arrangement
leads to a special construction of tetrahedral glasshouses,
where the short but strong spines mark the corners of thetetrahedron. Therefore, these glasshouses resemble concrete
breakwaters built by humans. They can be found, similar
to the star-sand of the West Pacific, in highest energetic
regions of the Indonesian Archipelago.
Ocher to olive-green gardeners with large, often flat
greenhouses, scientific name Nummulitidae
The last clan of today’s gardeners with transparent walls
also house diatoms acting as greenhouse plants. In contrast
to the calcarinid clan, they prefer the deeper regions of theThin section through Baculogypsinoides spinosus (size = 2.5mm; photo E. Iordanova).

shallow tropical sea, where the weak light enables theirplants to obtain positive photosynthetic rates. This allows－60－

SEM micrograph of a spine of Baculogypsina sphaerulata(scale bar = 0.1 mm).

a canal system to shorten the path from the surroundings

Living Baculogypsina sphaerulata (size = 2.3 mm).

of the glasshouse to the first chamber, where the regulation
center, the cell nucleus, is located.
A single group of clan members keeps the chamberheight more or less constant during growth (Nummulites).

SEM micrograph of Baculogypsina sphaerulata (body size
without spines = 1.2 mm).
Living Schlumbergerella floresina (scale bar = 1 mm); markthe difference between the dominating sexual generation (gamont)
and the single individual in the center belonging to the asexual
generation (agamont).

SEM micrograph of the shell surface of Baculogypsina
sphaerulata (scale bar = 0.01 mm) showing elevated transparent
pillars and numerous pores between.

the gardener to profit from the carbohydrates produced by
the microalgae. This relationship functions so well for all
nummulitids that they do not depend on additional food.
All glasshouse constructions start from an initial planof spirally arranged chambers within a plane. They possess

SEM micrograph of a gamont of Schlumbergerella floresina(body size = 2.3 mm; photo C. Baal).

－61－

SEM micrograph of an agamont of Schlumbergerella floresina(body size = 3.1 mm).

Living Nummulites venosus (size = 2 mm).

This arrangement is called a ‘spiral of Archimedes’.
Therefore, all chambers are of similar size. Chambers of
the last whorl overlap the former whorls on the lateral side;thus, only the last whorl is visible from outside, which is a
growth form known as involute.
These thick glasshouses can be found on sandy bottom
between 30 and 70 m in clear water of the central Indian
Ocean and the northern and central West Pacific.
Another group with similar glasshouse constructions
is differentiated from the first group by a stronger increasein chamber height (Operculinella). This leads to flat outerchamber parts in large individuals (up to 1 cm). They are
restricted to the tropical West Pacific, where they prefersandy bottom from 50 to 90 m depth.
Similar to the amphisteginids, there are groups with
SEM micrograph of Nummulites venosus (size = 2.2 mm).

similar glasshouse construction that changes depending
on water depth. All are characterized by papillae thatare located in rows above the septa which separate thechambers.
Two groups of gardeners living in shallower tropicalwater (but always below 20 m) construct thick tests. One
group makes discoid glasshouses, where only the last whorl
is visible (Operculina discoidalis). These gardeners prefersoft bottom such as found in tropical lagoons of the West
Pacific or in about 50 m depth in front of coral reefs.
The second group (Operculina ammonoides) is
distributed from the Red Sea to the West Pacific, startingat 10 m depth. In the Red Sea and Indian Ocean theseThin section of Nummulites venosus (size = 1.8 mm; photo E.
Iordanova).

－62－

SEM micrograph of Operculinella cumingii (size = 6.4 mm).

Living Operculinella cumingii (size = 10 mm).

Thin section of Operculinella cumingii (size = 1.3 mm; photo
E. Iordanova).

Light micrograph of Operculinella cumingii (size = 4.8 mm).

gardeners can live in deeper clear water down to 100 m,
where they construct large and flat glasshouses.
A third group with similar construction but elevatedsepta is restricted to fine sediments of the warm temperate
northwestern Pacific. It prefers 10 to 20 m depth.

Living Operculina discoidalis (size = 2.5 mm).

Similar forms with larger and flatter greenhouses live in－63－

SEM micrograph of Operculina ammonoides (size = 2.1 mm;
photo C. Baal).

SEM micrograph of Operculina discoidalis (size = 1.8 mm;
photo C. Baal).

Living Operculina ammonoides (size = 6 mm) from 60 m
depth.
Living Operculina ammonoides (size = 2.2 mm) from 20 m
depth.

found in clear tropical water at 120 m.
deeper regions of the East Indian Ocean and West PacificIn the deepest, light-depleted regions the glasshouses(Operculina complanata). All chambers are visible from theare extremely flat, very glassy and not as large as inlateral sides (evolute) and the chamber arrangement follows

shallower regions ( Operculina elegans). This helps thema ‘logarithmic spiral’, which means that the chambers

retain the smaller chamber size necessary for regulating

increase in height during growth.

chemical processes.

From 30 to 50 m depth the glasshouses are thick,A further modification to inhabit the deepest, light-

becoming extremely thin and flat with increasing depth.

depleted regions while keeping the large flat size and having

The deepest-living gardeners belonging to this group can besmall cytoplasm units to promote regulation and metabolic－64－Light micrograph of Operculina ammonoides from theNorthwest Pacific (size = 1.9 mm; photo C. Baal).

Living Operculina complanata (size = 4.8 mm).

SEM micrograph of Operculina ammonoides from theNorthwest Pacific (size = 2 mm; photo C. Baal).

processes, is to divide the strongly increasing chambers
by septula into smaller, equally sized compartments.
Two groups can be found, one where the division into
chamberlets is incomplete (Planoperculina) and anotherSEM micrograph of Operculina complanata (size = 4.3 mm).

where the division is complete (Planostegina).
All these gardeners are restricted to the tropical Indian

geographically and according to water depth. Thesegardeners are the only nummulitids with a worldwide

Ocean and West Pacific.
Similar to the last group, but with much thicker central

distribution. They are found in the Caribbean and in parts

test parts caused by the involute chamber arrangement,of the Mediterranean, where they intruded from the Red

are other gardeners (Heterostegina) that show the

Sea through the Suez Canal as so-called ‘Lessepsianwidest distribution range within the nummulitids, bothmigrants’. They are abundant in the whole tropical Indian－65－

Thin section of Operculina complanata (size = 2.2 mm; photo
E. Iordanova).

Living Planoperculina heterosteginoides (size = 3.5 mm).

Living Operculina elegans (size = 2.8 mm) from 100 m depth.

and Pacific Ocean and inhabit high energetic regions near
the reef crest, where they protect themselves in holes,
down to 70 m depth. At this depth, the glasshouses are flatand differentiated from the former relatives only by theirinvolute coiling in the glasshouse center.
The last two gardeners belonging to this group are
distinguished by the construction of large, flat and circularglasshouses. After an embryonic part (which differs in thetwo gardeners), the following constructions involving acyclic arrangement of similar-sized chambers are identical.
This leads to very large tests up to 13 cm, making them oneof the largest single-celled organisms in the world.
Their habitat depends on light availability and is locatedbetween 40 and 100 m depth. Both gardeners differ intheir initial part. While the first group － distributed in the
Indian Ocean－ shows a planspirally enrolled chamberarrangement in the initial part (Heterocyclina) , the second－66－

Living Planostegina longisepta (size = 3.2 mm).

SEM micrograph of the shell surface of Planostegina
operculinoides (scale bar = 0.1 mm) with small pustules.

SEM micrograph of Planostegina longisepta (size = 5.6 mm).

Thin section of Planostegina longisepta (size = 1.9 mm; photo
E. Iordanova).

SEM micrograph of Planostegina operculinoides (size = 3.3mm).

Living Heterostegina depressa (size = 3.4 mm).

group of gardeners － restricted to the tropical Pacific Ocean－ possesses a large embryonic part constituted of a few
chambers (Cycloclypeus) .

The fate of empty glasshouses
SEM micrograph of the shell surface of Planostegina
longisepta (scale bar = 0.1 mm).

－67－

What’s the fate of glasshouses when the gardeners leave

SEM micrograph of Heterocyclina tuberculata (size = 5.8 mm;
photo C. Baal).

SEM micrograph of Heterostegina depressa (size = 3.5 mm;
photo C. Baal).

Thin section of Heterostegina depressa (size = 3.2 mm; photo
E. Iordanova).

Living Cycloclypeus carpenteri (size = 7.8 mm).

Thin section of Cycloclypeus carpenteri (size = 8.2 mm; photo
E. Iordanova).
Light migrograph of Heterocyclina tuberculata (size = 5.8 mm;
photo C. Baal).

glasshouses will be transported. As opposed to normalthem either during reproduction or at death?

form and density of glasshouses determines the transport

sediment grains that are ellipsoidal or spherical, theFirst, the glasshouses lose their connection to the

distance: they are not as heavy as compact grains, andsubstrate where they were attached by the gardener’splate-like objects will be transported by fluids further thanpseudopods. This exposes them to water motion like otherspherical forms. In analogy, a tree leaf is transported more

sediment grains. Depending on the intensity, form (laminar

easily by wind compared to a compact fruit with the sameor turbulent flow) and direction of the water motion, thesevolume and weight as the leaf.

－68－Sandy beach west of Okinoerabu Island, Japan.

SEM micrograph of Cycloclypeus carpenteri (size = 8.5 mm;
photo C. Baal).

The empty glasshouses of extremely abundantcalcarinid gardeners on the reef crest are transported bywaves to the beaches, where they accumulate. This often
leads to large dunes consisting of sand with a significant
proportion of foraminiferal tests.
The spines of calcarinid tests are abraded, secondarily
during transport but primarily at the beach by oscillatory
wave action. This yields well-rounded calcite grains of afew mm size. Especially at the beaches of the Indonesian

Beach sand of Sesoko Island, Okinawa, Japan with numerous
rounded Calcarina shells (scale bar = 10 mm).

archipelago, when no human influence like pollution by
agriculture destroys the ecosystem, the beach sand consists
to more than 90% of well-rounded, equally sized calcareous
grains originating from gardeners living 100 m in front of
the beach. Such beaches are ideal tourist places.
When this beach sand is no longer moved by waves
and becomes stabilized, then the evaporation of sea water
between the grains leads to the precipitation of calcium
carbonate crystals that adheres the loose grains to one
another. This phenomenon is called cementation. It resultsin so-called beachrocks, which in this case consist mostlyof calcarinid glasshouses that can be preserved for further
millions of years.

Sand of Nusa Dua Beach, Bali, Indonesia consisting of morethan 90 % rounded Schlumbergerella tests (scale bar = 10 mm).

Less stabile plate-like glasshouses from gardeners livingin shallow water are also transported to the beach by wave

the waters down to 2000 m. Therefore, depending on slope

action, where they are fractioned and pulverized.

inclination and the size and form of the glasshouses, they

The less abundant gardeners living in front of the reef

can be transported. Size and shape determine transport

are mostly transported downslope, either through currents

distances even if the foraminifera belong to the same clan.

- very strong during low (ebb) tide - or by tropical storms.

Most of the sand in front of coral reefs down to 200 m

Such storms affect the seafloor with oscillatory movement

is composed in the West Pacific of larger foraminiferal

down to 50 m, while additional current flow can influence

tests. The proportion and composition of glasshouses in－69－

Sand from 10 m depth in front of Sesoko Island, Okinawa,
Japan with abundant empty shells of larger foraminifera together
with sea urchin spines, broken coral peaces and mollusk shells(scale bar = 1mm).

Beach rock at the coast west of Okinoerabu Island, Japan.

Details of the beach rock consisting of abundant Calcarina
tests.

the sand depends on the depth at which the gardener lived.
Therefore, in shallow water down to 50 m, glasshouses ofSand from 50 m depth in front of Sesoko Island, Okinawa,
Japan with abundant empty thick shells of larger foraminifera
together with broken coral peaces and mollusk shells (scale bar =1mm).

shallow-living species are abundant; here, they have a grain
size similar to other components of the sand originatingfrom organisms like corals, bivalves, gastropods and spinesof sea urchins.
The grain size becomes finer with increasing depth,
making empty glasshouses now much larger compared to‘normal’ grains. When storms affect sediments at these
depths, then the fine particles could be removed while thelarger particles remain and are compacted. This procedure
is called winnowing. It must be differentiated from sorting,where glasshouses of the two generations of the samegardener are unequally widely transported by water motion
and deposited at different places due to their differingbuoyancies. Winnowing explains the accumulation of a
species where glasshouses of both generations are present,

Sand from 80 m depth in front of Sesoko Island, Okinawa,
Japan with abundant empty thin and flat shells of larger
foraminifera together with broken coral peaces and mollusk shells(scale bar = 1mm).

like the stones of the Egyptian pyramids. Sorting, on
the other hand, is the main mechanism explaining the－70－

accumulation of a single generation － almost of the same

sediment hinders the penetration of pore waters, allowing asize － of gardener’s glasshouses.

better preservation of glasshouses in the fossil record.

All empty glasshouses, whether non-transported

According to these differences the preservation ofor transported, can be covered by sediment. When thislarger foraminifera from shallow turbulent waters is poor,

becomes petrified, they become part of the sedimentary

especially when the test consists of high-magnesium calcite.

rock. Often they are dissolved in coarse-grained sediments

Preservation is much better in deeper water and very good

due to the large pore space here: oxygenized pore waters

in fine-grained sediment.

lead to the solution of calcium carbonate. Here, aragonite

Sediments with larger foraminifera deposited in waterand high magnesium calcite tests are more affected thandepths from 20 to 50 m depth due to winnowing or sorting

those composed of low magnesium calcite. Fine-grained

are excellent reservoirs of hydrocarbons like petrol andpetroleum gas based on their large pore space. Thus, mostof the petrol reservoirs today are found in such limestone
mainly composed of larger foraminifera.
This leads to the question when and why in Earthhistory such accumulations of microscopic glasshouses
were formed.

The history of gardeners (Figure 8)
The foraminifera, the group of organisms to which thegardeners belong, show a long history. These single-celledorganisms are first documented with simple tests in theoldest rocks where other remains of organisms also appear
in high numbers. This is the Cambrian period about 540
million years ago. These oldest foraminifera remained
rather conservative with simple, single-chambered tubular
or spherical tests until the Devonian, where the firstchambered tests are reported. The Devonian is the lastperiod of the so-called Early Paleozoic time, ranging from
416 to 359 million years. This period is distinguished by ahigh proportion of land mass, which was important for the

Pleistocene outcrop west of Okinoerabu Island, Japan.

development of land plants. The first fish-like vertebrates
left the sea. In the shallow parts of the oceans surrounding
the large continents, the foraminifera developed different
types of tests. In the latest Devonian, beside agglutinatedand secreted walls － the latter made of fine globular
microcrystals － the first transparent (hyaline) walls
appeared. A bloom of the foraminifera in the following
period, the Carboniferous, parallels the development ofshallow marine organisms as well as plants and terrestrialorganisms. In the Late Carboniferous called Pennsylvanianand in the following Permian, the first gardeners within theforaminifera appeared, showing high evolutionary trends

Details of the Pleistocene outcrop west of Okinoerabu Island,
Japan (scale bar = 10 mm) with densely packed flat Planostegina
shells together with non rounded gravel of volcanic rocks.

in the Pennsylvanian and the Permian. These trends areused for time determination of the sediments in which theglasshouses are preserved.
The glasshouse construction of these earliest gardeners,－71－

Figure 7. Additional test constructions found in fossil larger foraminifera (Fusulina modified after Pokorny 1958, Neoschwagerina
modified after Dutkevitch 1932, Orbitolina modified after Douglass 1960).

－72－

Figure 8. Time distribution of the most important groups of larger symbiont-bearing foraminifera (colors corresponding to the symbiotic
microalgae, where symbionts of the extinct Fusulinidae and agglutinating foraminifera are unknown).

－73－known as fusulinids, is a spindle, similar to the spindleshaped alveolinids today.
The main characteristic of the glasshouse construction isthe division of the axially elongated chambers into smaller
compartments, especially when the glasshouse reacheda large size. This chamber division was obtained in two
ways (Figure 7). The first way was by folding the septum,
thus coming in contact with the septum of the former
chamber, or by dividing the chamber by horizontal andThin section of an Early Permian limestone (~ 305 Million
years ago) showing an equatorial section of Neoschwagerina to theleft and an axial section to the right (size ~ 5.5 mm; photo C. Baal).

The spindle shaped foraminifer Fusulina (size = 5.6 mm) fromthe Late Carboniferous (~ 308 million years ago; photo C. Baal).

The wall of Fusulinella (Late Carboniferous, ~ 310 million
years ago) in thin section showing a thick dark wall with an innerthin transparent layer that is called ‘Diaphanotheka’ (scale bar =0.1 mm; photo C. Baal).
Thin section of an Early Permian limestone (~ 270 million
years ago) showing an axial section of Parafusulina (size = 13mm). Mark the septal folding for dividing the large chambers into
smaller compartments (photo C. Baal).

The wall of Pseudoschwagerina (Early Permian, ~ 290 million
years ago) in thin section showing a thin dark outer layer and a
thick inner, still dark but more transparent layer, which is called‘Keriotheka’ (scale bar = 0.1 mm; photo C. Baal).
Thin section of a Late Carboniferous limestone (~ 305 million
years ago) showing an equatorial section of Triticites (size = 3.1mm; photo C. Baal).

－74－

vertical partition panels. Additionally, these gardeners canbe differentiated into two groups by their walls structure
named ‘diaphanothekal’ and ‘keriothekal’.
The role as gardeners can be proved based on thechemical composition of the walls. This composition
deviates from normal foraminiferal tests by a higher
content of heavy carbon isotopes (13C) compared with thenormal sea water, as can be measured in tests and shells ofanimals without symbiotic microalgae. This higher content
is characteristic for the glasshouses of living gardeners
because the cultivated plants inside the glasshouse use thelighter carbon isotope (12C) for photosynthesis. This left
only the heavier carbon isotopes in the cytoplasm and for

A Late Triassic (~ 205 Million years ago) limestone withnumerous Triasina specimens (scale bar = 1 mm; photo C. Baal).

use to construct the glasshouse walls consisting of calcium
carbonate (CaCO3). Nothing is yet known about the natureof the microalgae: they could have belonged to the green
or red algae, but also ancestors of the dinoflagellates are
possible.

An Early Permian (~ 270 Million years ago) fusulinid
limestone with numerous specimen of Pseudoschwagerina (scalebar = 1 mm; photo C. Baal).

Thin section of a Late Triassic limestone (~ 205 million yearsago) showing Triasina (diameter of the largest specimen = 1.8 mm;
photo C. Baal).

The cyclic larger foraminifer Orbitopsella (size = 6.6 mm)from the Early Jurassic (~ 170 million years ago) with a test wallconsisting of small agglutinated particles (photo C. Baal).

Equatorial section of Orbitopsella (diameter = 10 mm) showing
the cyclic arrangement of chambers (photo C. Baal).

－75－

Axial section of Orbitopsella (diameter = 9 mm; photo C.
Baal).

The flat conical, disc-shaped Orbitolina (size = 6.8 mm) from
the Middle Cretaceous (~ 97 million years ago; photo C. Baal).

Sandstone from the Late Cretaceous (~ 68 million years ago)
with the spindle-shaped foraminifer Loftusia (scale bar in mm;
photo C. Baal).

Axial section of Loftusia (length = 2 mm) showing the nontransparent walls made of agglutinated foreign particles (photo C.
Baal).

Axial section through Orbitolina (size = 4.6 mm) showing thenon transparent walls made of agglutinated foreign particles (photo
C. Baal).

After the catastrophic mass extinction at the end of thePermian 251 million years ago, the foraminifera needed
time to resettle the marine environment. They started in
the Early Triassic with forms similar to the representatives
with simple tests of the Early Carboniferous.
The rapid evolution during this period led to tests
similar to the type of today’s glasshouses that make pillars
instead of septula to strengthen the test (Triasina). This
phase was interrupted at the beginning of the Jurassic, theperiod in which the largest dinosaurs lived.
In shallow waters of the Early Jurassic until the Late
Cretaceous, some glasshouses with wall structures similar
to the Paleozoic forms－meaning composed of small andtiny granular microcrystals or constructed by collected sand

A Middle Cretaceous (~ 100 Million years ago) sandstone withnumerous Orbitolina specimens (scale bar = 1 mm; photo C. Baal).

particles fixed with calcareous cement － can be found. Their
test construction resembles either flat circular (Orbitopsella)or spindle-shaped glasshouses (Loftusia).
－76－

During the middle Cretaceous (125 to 93 million yearsago), the foraminifers with sandy test walls invented a(those with spindle-shaped glasshouses and porcellaneous
walls) appeared.

different way of constructing large-sized tests that cannot

They are accompanied by gardeners with circular

be compared with older or younger forms. These ‘architects’

glasshouses and transparent walls, where the chambers

got new ideas. They started with a chambered test, where

are arranged in cycles, similar to the two largest gardeners

after an initial and short planispirally coiled part theliving today. In contrast to these forms, these glasshouses

chambers were arranged in a straight series. By strongly

are not flat, but lens-shaped. This reflects the addition ofincreasing chamber width and reducing the planispiral partto a short embryonic part, these constructions became smallcones (Figure 7). The size increase during evolution was
obtained by reducing the cone height while at the same time
widening the chambers. The result: extremely flat, disc-like,large tests at the end of the Cretaceous (Orbitolina). Thesearchitects probably also housed symbiotic plants and thus
worked as gardeners.
In the Late Cretaceous, ancestors of living gardeners

Axial section through Orbitoides (size = 5.1 mm) showing
the large nepiont, the median layer and lateral chambers between
transparent piles (photo C. Baal).

The cyclic foraminifer Orbitoides (size = 3.3 mm) from the Late
Cretaceous (~ 67 million years ago; photo C. Baal).

Equatorial section through Orbitoides (size = 4.7 mm) showing
a large embryonic apparatus (nepiont) surrounded by an annulararrangement of chambers (photo C. Baal).

Equatorial section through Lepidorbitoides (size = 5.9 mm)from the Late Cretaceous (~ 67 million years ago) showing alarge embryonic apparatus (nepiont) surrounded by an annulararrangement of chambers. Mark the difference in the nepionts
between Orbitoides and Lepidorbitoides (photo C. Baal).

Thin section of a Late Cretaceous (~ 67 million years ago)sandstone with numerous axially sectioned Orbitoides specimens(scale bar = 1 mm; photo C. Baal).

－77－

lateral small chambers, similar to the construction of thetoday’s most developed star-sand gardeners. Also similar
to the living star-sand, they developed transparent plugs
or pillars to promote photosynthesis for algae living in the
inner parts of the glasshouses.

Axial section of the spindle shaped Alveolina (size = 6.3 mm)from the Middle Eocene (~ 45 million years ago) showing the dark,
porcellaneous, non transparent wall (photo C. Baal).

The cyclic foraminifer Orbitolites (size = 2.6 mm) from theMiddle Eocene (~ 45 million years ago; photo C. Baal).

Equatorial section through Orbitolites (size = 7.6 mm) showing
the non-transparent porcellaneous wall (photo C. Baal).
Equatorial section of Alveolina (size = 3.2 mm; photo C. Baal).

Thin section of a Middle Eocene (~ 45 million years ago)
limestone with numerous Alveolina specimens with dark, nontransparent walls (scale bar = 1 mm; photo C. Baal).

Thin section of a Middle Eocene (~ 45 million years ago)
limestone with numerous Orbitolites and Alveolina specimens withdark, non transparent walls and Nummulites specimens with bright,
transparent walls (scale bar = 1 mm; photo C. Baal).

－78－

This glasshouse construction was very successful,allowing the settlement of gardeners in a wide range of
habitats, from high energetic zones with intense water
motion down to the base of the photic zone with low lightintensities. These successful constructions were developed
independently by different clans of gardeners. They cannot
be differentiated from the outside, where all feature lensshaped glasshouses, but they differ strongly in their initialpart, the embryonic chambers called nepiont (Orbitoides,
Lepidorbitoides). According to evolutionary tendencies
from simple nepionts to complex forms, they can be used
to determine the deposition time of the sediments in whichthese forms are preserved.
After the second catastrophic mass extinction at the

Isolated Nummulites specimens washed from Middle Eocenemarls, showing the difference between sexual (small shells) andasexual (large shell) generations (scale bar = 2 mm; photo C. Baal).

end of the Cretaceous, where the dinosaurs and ammonites
disappeared, the development of the foraminifera was quite

The planispirally coiled foraminifer Nummulites (size = 4.7mm) from the Middle Eocene (~ 45 million years ago; photo C.
Baal).

Thin section of a Middle Eocene (~ 45 million years ago)
limestone with numerous Nummulites specimens with transparent
walls (scale bar = 1 mm; photo C. Baal).

Equatorial section through Discocyclina (size = 10.6 mm)from the Middle Eocene (~ 45 million years ago) showing alarge embryonic apparatus (nepiont) surrounded by an annulararrangement of chambers. Mark the difference in the nepiont andchamber arrangement to the Cretaceous species Orbitoides andLepidorbitoides (photo C. Baal).

Thin section of a Middle Eocene (~ 45 million years ago)
limestone with numerous axially sectioned Discocyclina specimens(scale bar = 1 mm; photo C. Baal).

－79－

similar to their evolution after the first mass extinction.
Starting from surviving forms with simple tests, theforaminifera soon developed gardeners in different
lines. Precursors and ancestors of all living gardeners
started in the Paleocene, the first epoch of the Cenozoic.
Beside the recurrence of spindle shaped glasshouses withporcellaneous walls (alveolinids), a phenomenon known asa Lazarus effect, the soritids (Orbitolites) and archaiasinids
appeared, settling in the shallowest, most light-intensive
regions.
The main evolution took place in the newly developed
nummulitids. They constructed planispiral glasshouses withtransparent walls that reached immense abundances andsizes (up to 17 cm) between 55.8 to 37.2 million years ago,
belonging to the Eocene epoch. Sediments with enormous
The cyclic foraminifer Miogypsina (size = 3 mm) from the
Early Miocene (~ 20 million years ago; photo C. Baal).

Equatorial section through Lepidocyclina (size = 2 mm)from the Late Oligocene (~ 27 million years ago) showing alarge embryonic apparatus (nepiont) surrounded by an annulararrangement of chambers. Mark the difference in the nepiont andchamber arrangement to the Eocene Discocyclina (photo C. Baal).

Axial section through Lepidocyclina (size = 1 mm; photo C.
Baal).

Equatorial sections of Miogypsina (scale bar = 1 mm) showing
the embryonic apparatus that does not lay in the center. Mark theevolution in the nepiont from a planispiral arrangement to a typicalmiogypsinid nepiont (photo C. Baal).

－80－

chambers by septula into smaller chamberlets. Circularforms were then developed in the youngest Earth period.
Today, the extreme pollution and destruction ofshallow-water environments in the oceans endanger theglasshouse gardeners, which need clear, nutrient-poor sea
water and abundant light for survival. Global warming,
without pollution, would promote the development ofglasshouse gardeners. Huge carbonate buildups could be
produced in the future, replacing coral reef growth. The
latter do not like higher water temperatures, as is evident
in the lack of carbonate buildups made by corals during
Thin section of an Early Miocene (~ 20 million years ago)sandstone with numerous Miogypsina specimens (scale bar = 1
mm; photo C. Baal).

the high temperatures in the Paleogene, when carbonate
buildups by larger foraminifera dominate. Despite this good
prognosis for gardeners reacting to global warming, they
are endangered by high pollution, the acidification of theoceans and the many forms of habitat destruction caused byhuman activities.

Thin section of a Pleistocene (~ 1.5 million years ago)
limestone with numerous Cycloclypeus specimens together with
Baculogypsinoides and Amphistegina (scale bar = 1 mm; photo C.
Baal).

amounts of nummulitids are today’s largest oil reservoirs,
and the stones of the pyramids also belong to this epoch.
Glasshouses with cyclic chamber arrangement
and lateral chambers that were successful in the Late
Cretaceous were still constructed in the older Cenozoic
period, the Paleogene. But they originate from different
groups of foraminifera compared to the Cretaceous forms(Discocyclina).
There was a strong environmental change at theend of the Eocene epoch, leading to a size decrease in
nummulitids. This also corresponds to the development of
new cyclic gardeners (Lepidocyclina, Miogypsina).
Both groups survived the boundary between the
Paleogene and Neogene 23.03 million years ago andsurvived until 15.97 million years ago. Then, glasshouse
constructions with lateral chambers disappeared and were
replaced by nummulitids dividing their strongly increasing－81－

Indexitalic: in photograph and f igure explanation
Achatna, 5Belau, 37, 46

Achnanthes, 19benthic, 4, 8, 18, 35

Acropora, 39

benthonic, 4agamont, 8, 10, 11, 15, 36; 61, 62

biomineralization, 23

alkaline, 13, 22

Borelis melo, 51

Alveolina, 31, 78

Calcarina, 39, 69, 70

Alveolinella, 51; 40

Calcarina calcar, 54; 39, 55

Alveolinella quoyi, 41, 50, 51

Calcarina defrancii, 55; 56

Alveolinidae, 50

Calcarina gaudichaudii, 55; 34, 39, 57

amino acid, 6, 12

Calcarina hispida, 56; 41, 58, 59

Ammonia, 24

Calcarina mayori, 56; 42, 59

ammonite, 4, 5, 27, 79

Calcarina quoyi, 56; 58

ammonium (NH4), 13

Calcarinidae, 53

amoeba, 4, 24

calcite, 6, 23, 69, 71

amorphic, 22

calcium (Ca), 13

Amphisorus, 49; 10, 15, 18, 37, 38, 39

calcium carbonate (CaCO3), 1, 14, 22, 23, 69, 71, 75

Amphisorus hemprichii, 41, 49, 50

Cambrian, 71

Amphistegina, 52, 53; 20, 40, 41, 81

canal, 27, 28, 34, 50, 61; 28

Amphistegina bicirculata, 52; 33, 53

Cape Bise, 37

Amphistegina lessonii, 52; 32, 52

carbon (C), 13, 14, 18, 19, 22, 36

Amphistegina lobifera, 52; 21, 32, 39, 52

carbon acid (H2CO3), 13

Amphistegina papillosa, 52; 33, 41, 42, 53

carbon dioxide (CO2), 6, 8, 12, 13, 18, 21, 22, 23

Amphistegina radiata, 52; 32, 41, 42, 53

carbon isotope (12C), 75

Amphisteginidae, 52

carbon isotope (13C), 75

Amphora, 19

carbonate (CO32-), 1, 13, 14, 22, 23, 36, 69, 71, 75, 81

annular, 29, 46; 77, 79, 80

Carboniferous, 71, 76 ; 74

aperture, 24, 27, 28, 30, 37, 38, 45, 49, 50, 55; 5, 21, 29,

Caribbean, 46, 47, 65

43, 48, 49, 50, 51

carotin, 12

Archaias, 46; 29

catabolism, 13

Archaias angulatus, 47

cellulose, 12, 17

Archaiasinidae, 45

cementation, 15, 69

asexual reproduction, 15, 18, 19, 35

Cenozoic, 80

ATP (adenosine triphosphate), 8, 13, 21

Central Pacif ic, 46, 49, 54, 62

axis of rotation, 2

cephalopods, 2, 4, 5, 24; 6

Bacillariophyta, 18

chamberlet, 28, 29, 30, 47, 49, 50, 65, 81; 29

backreef, 46

Chlamydomonas, 16, 17, 19, 45; 16, 17

Baculogypsina, 39

chlorophyll a, 12, 15, 16, 17, 19

Baculogypsina sphaerulata, 35, 39, 61

chlorophyll b, 12, 16, 17, 19

Baculogypsinoides, 56; 81

chlorophyll c, 12, 15, 17, 19

Baculogypsinoides spinosus, 34, 42, 60

Chlorophyta, 16Bali, 69

chloroplast, 11, 12, 18; 11, 16, 17, 18, 20

beachrock, 69; 70

chromosomes, 8, 10; 18－83－

ciliate, 20

fossilization, 2

Cocconeis, 19

Fragilaria, 19

coenzyme, 13

frustulum, 19; 19

compartment, 6, 8, 21, 24, 27, 28, 65, 74; 74

fucoxanthin, 12

compensation depth, 36, 41, 42

fusiform, 30

coral bleaching, 36

Fusulina, 72, 74

Corallinacea, 15

Fusulinella, 74

Cretaceous, 76, 77, 79, 81; 76, 77, 79

gamete, 8, 10, 15, 16, 35; 9cyclic, 29, 30, 34, 66, 81; 29, 75, 77, 78, 80

gamont, 8, 10, 11, 35; 61

Cycloclypeus, 36, 81

glucose, 12

Cycloclypeus carpenteri, 68, 69

glycerol, 12, 16, 18, 20; 11

Cyclorbiculina compressa, 47

Golgi vesicles, 6, 23

cytoplasm, 6,11, 12, 14, 15, 18, 20, 21, 22, 27, 35, 51, 64, 75

habitat, 43, 66, 79, 81

dendritic, 42, 45; 43

Halimeda, 38

Dendritina, 43; 16, 21, 43

Haploid, 8, 10, 11

Dendritina ambigua, 43, 44

Hateruma, 39, 54

Dendritina zhengae, 43, 44

Heterocyclina, 66; 29

detritus, 6, 8, 21

Heterocyclina tuberculata, 68

Devonian, 71

Heterostegina, 65; 41

diaphanotheka, 75; 74

Heterostegina depressa, 42, 67, 68

diatom, 6, 8, 18, 19, 20, 22, 36, 51, 52, 53, 60; 19, 20

high magnesium calcite, 23, 71

dictyosome, 6, 23, 28

hyaline, 24, 35, 41, 51, 71; 24

digestion, 6, 13hydrocarbon, 71

dinoflagellate, 6, 17, 18, 19, 36, 48, 75; 18hydrogen (H+), 12, 13

diploid, 8, 11, 15hydrogen carbonate (HCO3－), 14, 36

Discocyclina, 81; 79, 80

Indian Ocean, 49, 51, 54, 62, 64, 65, 66

DNA = Deoxyribo Nucleic Acid, 8, 12, 30

Indonesia, 54, 60, 69; 69

dune, 69

inorganic carbon, 8, 13, 14, 18, 22

dysphotic, 19

involute, 30, 62, 65, 66

East Indian, 54, 64

iron (Fe), 13, 22

ectoplasm, 8

Ishigaki, 38, 39

egg-holder, 21; 22

isogamete, 8, 10, 16, 35

embryonic apparatus, 30, 35; 77, 79, 80

Jania, 38

endoplasm, 8

Jurassic, 28, 76; 75

endoplasmatic reticulum, 6

lagoon, 42, 49, 51, 62; 37, 42, 46

endoskeleton, 2, 22

lamella, 32, 33, 34, 35

endosymbiont, 19; 17

Kabira Bay, 38, 39

Enhalus, 37

keriotheka, 75; 74

Entomoneis, 19

Laevipeneroplis, 45

enzyme, 6, 13, 15

Laevipeneroplis proteus, 45, 46

Eocene, 80, 81; 78, 79, 80

Lazarus effect, 80

equatorial section, 2; 4, 74, 75, 77, 78, 79, 80

Lepidocyclina, 81; 80

euphotic zone, 8, 19

Lepidorbitoides, 79; 77, 79

flagellum, 17, 35

Lessepsian migrant, 65

foramen, 5, 27, 50

life span, 8, 10, 11, 27

foraminìfera, 5, 6, 8, 10, 11, 12, 14, 15, 16, 17, 18, 19, 20,

lipid, 6, 8, 12, 18, 20; 11

22, 23, 24, 28, 30, 35, 36, 38, 42, 69, 71, 76, 79, 80, 81

living sand, 54; 39, 54－84－

lobopod, 4nutrient, 11, 13, 14, 16, 20, 21, 27, 81

Loftusia, 76; 76

Okinawa, 37, 38, 39, 40, 41, 42, 54, 69, 70

logarithmic spiral, 27, 64; 28, 29

Okinoerabu, 69, 70, 71

low (ebb) tide, 69

Oligocene, 80

low magnesium calcite, 23, 71

opal (SiO2・nH2O), 22

lysosomes, 15, 28

Operculina, 62, 64; 22, 24, 28, 41

macroalgae, 37, 38, 43, 46, 48, 55

Operculina ammonoides, 62; 27, 64, 65

macroids, 41

Operculina complanata, 64; 42, 65, 66

macropolymere, 6

Operculina discoidalis, 62; 42, 63, 64

magnesium (Mg), 13, 23

Operculina elegans, 64; 66

magnesium carbonate (MgCO3), 23

Operculinella cumingii, 63

mannitol, 17

optical axis, 22, 23, 24

Marginopora, 50

Orbitoides, 79; 77, 79

Marginopora vertebralis, 50

Orbitolina, 77; 72, 76

maximum survival temperature (MaxST), 36

Orbitolites, 80; 78

Mediterranean, 43, 49, 65

Orbitopsella, 76; 75, 76

meiosis, 8, 10

organic carbon, 18, 19

membrane, 6, 8, 11, 12, 15, 16, 17, 35

oxygen (O), 6, 8, 12, 21, 23

metabolism, 8, 20, 24, 36

Paleocene, 80

microalgae, 6, 8, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21,

Paleogene, 81

22, 24, 30, 33, 35, 36, 37, 42, 48, 51, 52, 56, 61, 75; 11,

Paleozoic, 71, 76

14, 16, 17, 18, 38, 44, 73

papilla, 33, 52, 62; 33

Micro-Einstein, 19

Parafusulina, 74

microf ilaments, 8

Paramecium, 8, 20

minimum survival temperature (MinST), 36

Parasorites, 46; 17

Miocene, 80, 81

Parasorites orbitolitoides, 41, 47, 48

Miogypsina, 81; 80, 81

Peleliu, 37, 46

mitochondria, 8, 10, 21, 28; 11, 16, 20

Peneroplidae, 42

Motobu, 37, 42, 54

Peneroplis, 5, 6, 28, 29, 38, 39mRNA (messenger Ribo Nucleic Acid), 8

Peneroplis antillarum, 43; 39, 44

Nautilus, 4, 5, 24, 27; 5, 6

Peneroplis pertusus, 27, 43; 43, 45

Navicula, 19

Peneroplis planatus, 43, 46; 43, 44

nektonic, 4Pennsylvanian, 71

Neogene, 81

Permian, 71, 76; 74, 75

Neorotalia, 10

petrol, 71

Neoschwagerina, 72, 74

petroleum gas, 71

nepiont, 30, 79; 29, 77, 79, 80

phagocytosis, 15

net production, 36

phagosome, 6, 15

nitrate (NO3), 13

phospholipids, 6, 12

nitrogen (N), 12, 14, 21

phosphoric acid, 13

nucleic acid, 8, 12

phosphorus (P), 12, 13, 14, 21

nucleus, 8, 11, 15, 21, 23, 28, 30, 35, 61; 11, 17, 18, 20

photic zone, 19, 79

Nummulites, 2, 27, 61; 28, 78, 79

photoinhibition, 36

Nummulites perforatus, 2

photon, 19

Nummulites venosus, 62

photosynthate, 16, 17, 18, 20, 21

Nummulitidae, 62

photosynthesis, 8, 11, 12, 13, 14, 16, 17, 18, 19, 21, 22, 24,
32, 33, 34, 35, 36, 47, 51, 52, 75, 78; 11

Nusa Dua, 69－85－

phycobilin, 12, 15

Sesoko, 38, 39, 40, 41, 69, 70

phycoerythrin, 15

sexual reproduction, 10, 15, 18, 35

phytoplankton, 8, 11, 13, 17, 18, 19

silicic acid (SiO2), 18, 22

pile, 35, 77

sipho, 5pillar, 28, 35, 46, 76, 78; 29, 61

Sorites, 48; 29

planispiral, 2, 24, 29, 30, 45, 50, 60, 77, 80; 3, 5, 26, 79, 80

Sorites orbiculus, 48

planktic, 8, 10, 18

Soritidae, 48

plankton, 8, 35

sorting, 70

Planoperculina, 65

spike, 55, 56; 57, 58

Planoperculina heterosteginoides, 66

spine, 8, 33, 34, 38, 40, 53, 54, 55, 56, 57, 60, 69, 70; 34,

Planostegina, 65; 14, 71

35, 55, 56, 57, 58, 59, 60, 61, 70

Planostegina longisepta, 66, 67

spiral of Archimedes, 27, 28, 30, 62; 27

Planostegina operculinoides, 67

spiral side, 30

plastid, 11, 15, 16, 17

star sand, 54, 55, 60, 78; 54

Pleistocene, 71, 81

starch, 12, 17

plug, 32, 52, 56, 78; 32

stolon, 28, 29; 22, 29

porcellaneous, 30, 36, 42, 45, 47, 48, 50, 51, 77; 23, 44, 78

streptospiral, 24

pore, 23, 27, 45, 47, 71; 24, 57, 58, 61

sulfur (S), 12, 13, 14Porphyridium, 16

Symbiodinium, 18, 19; 18Porphyridium purpureum, 15, 16

symbiont, 12, 13, 14, 15, 16, 17, 18, 19, 21, 23, 27, 33, 36,
48, 51; 18, 73

potassium (Ka), 13
primary producer, 18

symbiosis, 11, 13

proloculus, 24

symbiosome, 15, 16

protein, 6, 8, 12, 13, 17, 27

TEM (transmission electron microscope), 11; 11, 16, 17, 18, 20

Protokeelia, 19

Thallus, 38

pseudopod, 4, 11, 20, 21, 30, 32, 37, 38, 43, 51, 68; 5

Triasina, 76; 75

pseudopore, 43

Triassic, 76; 75

Pseudoschwagerina, 74, 75

Triticites, 74

pustule, 33, 56, 57; 67

trochospiral, 4, 24, 30, 32, 33, 34, 52, 53, 54

Pyrrhophyta, 17Ulva, 12

Quinqueloculina, 23

umbilical side, 30, 32, 52

radiolaria, 22

upwelling, 13

Red Sea, 13, 49, 51, 62, 65

UV (ultra violet), 17, 23, 30, 32, 36

reef crest, 15, 30, 43, 51, 54, 55, 56, 66, 69; 37, 39, 54

vacuole, 11, 17; 11, 17, 18, 20

reef crown, 37, 38, 39, 40

West Atlantic, 49

reef moat, 46, 51; 37, 38, 39

West Pacif ic, 46, 47, 49, 51, 54, 60, 62, 64, 65, 69; 65

reef slope, 30, 40, 43, 51, 56, 57; 40, 41, 42

winnowing, 70

reproduction, 8, 10, 11, 14, 15, 16, 17, 18, 19, 35, 68

xanthophyllid, 12

respiration, 6, 8, 12, 18, 19, 21, 23, 36

zooxanthellae, 17, 18, 36

reticulopod, 4, 5, 8, 20, 21

zygote, 8, 10, 35

rhizomes, 37
Rhodophyta, 15
ribosomes, 6, 28
Rose Bengal, 11
Schlumbergerella, 69
Schlumbergerella floresina, 61, 62
septum, 50, 52, 74－86－