Experiences in Integrative and Comparative Biology
In this newsletter, we hear about some experiences from two former presidents of our Society, Al Bennett and Edwin Cooper. Edwin Cooper was president in 1983 and is a Distinguished Professor of Neurobiology in the David Geffen School of Medicine at UCLA. Al Bennett was president in 1990 and is a Professor of Ecology and Evolutionary Biology and Dean of the School of Biological Sciences at UC Irvine. Drs. Cooper and Bennett served as presidents when we were the American Society of Zoologists and when presidential terms were for one year instead of the current two year terms. I hope you enjoy some of the experiences these distinguished scientists share with us.
Lou Burnett, SICB Secretary
Boyhood Memories Imprinted
Laboratory of Comparative
Department of Neurobiology
David Geffen School of Medicine
University of California, Los
I remember recognizing early on
my fate to become a biologist-a zoologist. A lot of keen
observations actually stayed with me and contributed enormously to
shaping my career. In Houston Texas, where I grew up, spring rains
unearthed a wealth of animals that I found most fascinating.
Earthworms are not well when they are waterlogged so that excess rain
brought them out seeking penetrable but not soggy soil. I never
learned or liked to fish, instinctively not wanting to sacrifice
earthworms to serve as bait for a sport about which I had no
interest. Little did I know that earthworms would become one focus
of my life's work as a comparative immunologist demonstrating in
them in the early 1960s for the first time that an invertebrate could
destroy a transplant, heralding the field of invertebrate immunology
and rattling the monolithic world of immunology-much like
Metchnikoff did when he discovered phagocytosis down by the seashore
in southern Italy in Messina to be precise.
Visits to my maternal
grandfather's farm further piqued my fascination with earthworms.
As he plowed fields for planting, I became increasingly interested in
earthworms as tillers of the soil. Grandfather Porche even told me
that they would regenerate should his plow split them! There was
even more barnyard biology at the farm as I actually saw what later
became widely accepted in ethology as imprinting. Sneaking in and
out of the barn, I saw how young chicks would follow the mother hen
responding to her clucks. Or I saw his beehives and the dancing
When I did my early work, the
world of immunology was no more receptive than it was with
Metchnikoff. As open as scientists seem or profess to be, rocking
the boat is not always greeted with cheers! Persistence was
important to Metchnikoff and it was to me as well. Returning from
immunology meetings I became more convinced that I was on the right
track with my discovery of graft rejection. And I was not alone
since this observation had been made by the Germans in the 1920s.
Graft rejection in earthworms to them was a developmental phenomenon,
mediated by "individuality differentials" so well explained in
Leo Loeb's book: The Biological Basis of Individuality. This was
different from my interpretation-the self not self-concept,
governed my interpretations as did all of immunology following the
credo of Nobel Laureate Sir MacFarlane Burnet. Following his
immunologic surveillance idea, some still ponder how efficient is the
invertebrate immune response since there is relatively little
incidence of cancer in invertebrates. Then simultaneously with my
own seemingly independent work, the French School of emerging
comparative immunologists notably in Bordeaux (DuPasquier, Valembois
and his student Philippe Roch-later my post doc, winner of the
First von Behring Metchnikoff Prize in Immunology awarded by the
Societe Francaise d'Immunologie) were also thymectomizing frog
larvae and grafting earthworms!
Later in my career, my earlier
barnyard interest in observing nature was translated into watching
and documenting the effects of aggressive behavior in the edible fish
Tilapia and how the response to aggressive encounters could
depress the immune system-the beginnings of
psychoneuroimmunology-and other evidence that there are connections
between the immune, nervous and endocrine systems, through cross-talk
and sharing of cell markers such as receptors and mediator molecules.
Much later at UCLA I actually received funding from Norman Cousins
(first Editor of Saturday Review and a popularizer of self
healing), since he was interested in behavior. To my advantage I
assembled an international team and published a lot on an altered
immune responses in β or subordinate fish after exhaustive chasing and biting and ramming
by the α or
dominant fish. Our movies show this clearly and even when a single
fish is allowed to confront itself in a mirror, it will recognize
itself and do the very same attack strategies and attempt to defeat
it showing the same behavioral moves! When seemingly frustrated,
that single fish will suspiciously cast a gaze: frustrated trying to
figure a next winning move?
Back to Houston and rains, what
else did I see as a boy-the houses of crayfish, those piles and
piles of mud sticking up like primitive mud houses, or in puddles,
tadpoles that eventually sprouted legs and became frogs? Later my
explorations would lead to a complete dissection of the immune system
of the frog-the discovery of the thymus, lymph glands connected to
gills that, because of their structure, clean up blood and provide a
source of antibody-producing lymphocytes. Even more in the frog,
with a high school student, we showed the presence of stem cells in
bone marrow and their capacity to restore an immune system damaged
severely by irradiation.
I received the BS cum laude
in Biology from Texas Southern University in 1957 and was awarded a
scholarship to Atlanta University for the MS in Biology. In 1958, I
was accepted in the invertebrate zoology course at the Marine
Biological Laboratory in Woods Hole and did a project centrifuging
the eggs of Chaetopterus, a marine annelid, (ideas from the
early embryologist Dreisch: 1867-1941). I remember seeing the
quotation of Louis Agassiz: "Study Nature Not Books!" I returned
to Atlanta University and finished up my MS thesis in 1959 on
differentiation of the embryonic chick otocyst on the chorioallantoic
membrane of older chick embryos.
Clearly I had demonstrated a
measure of focus that changed drastically after I had arrived eagerly
in 1957. I had been so excited and had decided to do about 15
projects for my thesis! My major Professor Mary L. Reddick, Phi Beta
Kappa and PhD. Harvard (student of Leigh Hoadley, zoologist and
marine biologist) did her thesis on ear development in chicks. So in
1957 when I entered her office with my not so short list of proposed
projects, she tore it into pieces, smoked her Lucky Strike and said
in firm terms, "Mr. Cooper you will work on this!" (chick otocyst
From Reddick's sharp ultimatum,
(still did not daunt my enthusiasm and questioning at the ripe old
age of 20 years!) I had learned then immediately before arrival at
Brown in 1959 (finished the PhD in 1962) to sharpen my focus and
quickly chose to work with Professor Richard J. Goss (another Harvard
PhD in zoology and an authority on stem cells and regeneration in any
animal that upon amputation of a part would grow it again: salamander
limbs and deer antlers). No one had done one intriguing project that
excited me tremendously. So I decided to try and grow the salamander
regeneration blastema in tissue culture. However there was one
interruption in the tissue culture experiments that proved to be
beneficial and a major turning point that determined the course of my
career. Goss had plans for me to live in a glass house in Maine.
Spending a couple of summers with
Richard Goss at the Mt. Desert Island Biological Lab, Salisbury Cove,
Maine was fruitful. On a foggy day in the summer of 1961, Goss
shocked me to no end essentially withdrawing me from my blastema
project and urging me that upon returning to Brown in the fall, to
continue the immunosuppression project. Although hurt and
disappointed and feeling faint that my unique work had been
destroyed, I followed his advice, completed the project, later
published in the journal Transplantation and finished Brown on
time. Goss gave me two admonitions: he wanted me to finish a
project, not stay on for my PhD forever and not do a thesis that
needed to be wheeled in! -the blastema work was only giving me
enough positive results to keep me enthused, but not convinced. Of
course I was egged on at Developmental Biology Meetings, where I was
encouraged to continue by greats in embryology like the late
Professor Paul A.Weiss, Rockefeller University (formerly Rockefeller
Institute for Medical Research).
Finishing up my Ph.D., I mulled
the future. What kind of post-doc would I do? I thought -
developmental biology? No because the blastema project had not been
convincing and I was not sure about immunology, entering it without
ever having had a course-modern immunology was not yet exploding as
it has done since. Then one day in the Brown U library, I met Jane
Oppenheimer, the embryologist (Fundulus! embryos were included
on the 1975 Apollo-Soyuz space shuttle mission) and former president
of ASZ, chatted with her in the stacks and she mentioned the thymus
I quickly thought why not? At
that time, the current immunology explosion was just beginning with
people removing the thymus in mice, rats, even opossums primarily by
Jacques Miller. So I thought, thymus in fish, maybe also thymus in
tadpoles and immunosuppression and all was beginning to gel.
Before leaving Brown, I prepared
a post doc application to NIH (National Cancer Institute) and drove
west to California to work with William Hildemann at UCLA. Although
the proposal was for immunosuppression in fish, I actually wanted to
thymectomize bullfrog larvae to suppress their immune response. But
remembering my earthworms, I knew that they had no thymus, an organ
of vertebrates, but surely they had to have some kind of immune
response because they lived in soil-never mind the habitat. I
reasoned that all living creatures should be able to defend
themselves. So I dreamed: I will exchange skin grafts in earthworms
to show rejection as others were doing in birds, mice and rats. Once
again I was right. My sure project was the tadpole immune project,
grafting and showing antibody synthesis-the bread and butter as
Hildemann called it. Why? No one wanted to believe that I was
demonstrating graft rejection in earthworms, so Hildemann was
The American Society of
Zoologists was a natural outlet for my interests and energy. Later I
became involved with the International Society of Developmental and
Comparative Immunology, serving as its president and editor of its
journal, Developmental and Comparative Immunology. I am now
working to bring the SICB along as a corporate member of the
International Society of Zoological Sciences, which will be convening
a Congress in Paris in August 2008.
Cooper E. L. and Aponte, A. Chronic allograft rejection in the iguana, Ctenosaura pectinata. Proc. Soc. Exp. Biol. Med. 1968; 128: 150-154.
Cooper E. L. The effects of
antibiotics and x-irradiation on the survival of scale homografts in
Fundulus heteroclitus. Transplantation 1964; 2: 2-20.
Cooper, E. L. 1968.
Transplantation immunity in Annelids. I. Rejection of xenografts
exchanged between Lumbricus terrestris and Eisenia foetida.
Transplantation 6: 322-337.
Baculi B. S., Cooper E. L.
Lymphomyeloid organs of Amphibia. II. Vasculature in larval and
adult Rana catesbeiana. J Morphol. 1967; 123: 463-480.
Cooper E. L. Lymphomyeloid
organs of Amphibia. I. Appearance during larval and adult stages of
Rana catesbeiana. J Morphol. 1967; 122: 381-398.
Cooper E. L,
Garcia-Herrera F. 1967. La organización de un laboratorio de
investigación en embriologia e inmunologia comparada. Acta
Med. 3: 59-67.
Cooper, E. L. and Schaefer, D. W.
1970. Bone marrow restoration of transplantation immunity in the
leopard frog Rana pipiens. Proc. Soc. Exp. Biol. Med.
Hostetter, R. K. and Cooper, E.
L. 1973. Cellular anamnesis in earthworms. Cell. Immunol.
Ramirez, J. A., Wright, R. K.,
and Cooper, E. L. 1983. Bone marrow reconstitution of immune
responses following irradiation in the leopard frog Rana pipiens.
Dev. Comp. Immunol. 7: 303-312.
Hildemann, W. H. and Cooper, E.
L. 1963. Immunogenesis of homograft reactions in fishes and
amphibians. Fed. Proc. 22: 1145-1151.
Cooper, E. L. and Hildemann, W.
H. 1965. The immune response of larval bullfrogs (Rana
catesbeiana) to diverse antigens. Ann. N.Y. Acad. Sci.
Cooper, E. L. 1967. Some
aspects of the histogenesis of the amphibian lymphomyeloid system and
its role in immunity. In: Ontogeny of Immunity, eds. R. T.
Smith, R. A. Good and P. A. Miescher, Gainesville, University of
Florida Press, 87-102.
Cooper, E.L. Comparative
immunology. 1985. Past Presidential Address. Am. Zool. 25:
Cooper, E.L., Klempau, A.E. and
Zapata, A.G. 1985. Reptilian Immunity. In Biology of the
Reptilia, eds. C. Gans, F. Billett and P.F.A. Maderson, 600-678,
New York, John Wiley and Sons.
Cooper, E.L., Wright, R.K.,
Stein, E.A., Roch, P.J. and Mansour, M.H. 1987. Immunity in
earthworms and tunicates with special reference to receptor origins.
In Invertebrate Models, Cell Receptors and Cell Communication,
ed. A.H. Greenberg, 79-103, New York, Karger.
Mansour, M. H. and Cooper, E. L.
1987. Tunicate Thy-1 an invertebrate member of the Ig superfamily.
In Developmental and Comparative Immunology, Eds. E.L. Cooper,
C. Langlet and J. Bierne, 33-42, New York, Alan R. Liss.
Mansour, M. H., Negm, H. I. and
Cooper, E. L. 1987. Thy-1 evolution. Dev. Comp. Immunol.
Cooper, E. L. and Faisal, M.
1990. Phylogenetic approach to endocrine immune system
interactions. In Unconventional vertebrates as models in endocrine
research. eds. G.V. Callard and I.P. Callard, J. Exptl. Zool.,
Suppl., 4: 46 52.
Cooper, E. L. 1992. Innate
immunity. In Encyclopedia of Immunology, eds. I.M. Roitt and
P.J. Delves, 867-870, Jovanovich, Harcourt Brace Inc.
Cooper E. L. 1993. Basic
concepts and the functional organization of the immune system. In
Developmental Immunology, eds. E.L. Cooper and E.
Nisbet-Brown, 3-30, New York, Oxford University Press.
Cooper, E. L. Mansour, M. H. and
Negm, H. I. 1996. Marine invertebrate immunodefense response:
molecular and cellular approaches in tunicates. Ann. Rev. Fish
Dis. 6: 133-149.
Cooper, E. L. 1997. Comparative
Immunology of the Integument. In Skin Immune System, ed. J.
D. Bos, 18-39, Boca Raton, CRC Press.
Cooper, E. L., Kauschke, E. and
Cossarizza, A. 2002. Digging for innate immunity since Darwin and
Metchnikoff. Bioessays 24: 319-333.
de Eguileor, M, Tettamanti, G.,
Grimaldi, A. Ferrarese, R. Perletti, G., Valvassori, R., Cooper, E.
L. Lanzavecchia, G. 2002. Leech immune responses: contributions and
biomedical applications. In: Cooper EL, Beschin A, Bilej M, editors.
A new model for analyzing antimicrobial peptides with biomedical
applications. Amsterdam: IOS Press: 2002, 93-102.
Cooper, E. L. 2003 Comparative
immunology of the animal kingdom. In The New Panorama of Animal
Evolution, Proceedings XVIII International Congress of Zoology,
eds: A. Legakis, S. Sfenthourakis, R. Polymeni and M.
Thessalou-Legaki, Pensoft, Sofia, 117-125.
Cooper E. L. Comparative
Immunology. Integr Comp Biol 2003; 43: 278 - 280.
Rosas, C., Cooper, E. L.,
Pascual, C., Brito, R., Gelabert, R., Moreno, T., Miranda, G. and
Sánchez, A. 2004. La condición reproductiva del
camarón blanco Litopenaeus setiferus (Crustacea;
Penaeidae): Evidencias de deterioro ambiental en el Sur del Golfo de
México. In.: Diagnóstico ambiental del Golfo de México,
Secretaria de Medio Ambiente y Recursos, Instituto Nacional de
Ecología, Instituto de Ecología, eds. M. Caso, Irene
Pisanty y Ezequiel Ezcurra, 789-822, Mexico, A.C., Harte Research
Institute for Gulf of Mexico Studies, Vol. 2.
Cooper, E.L. (ed.) 1974.
Invertebrate Immunology. Contemporary Topics in Immunobiology
Vol. 4. New York: Plenum Press, 299 pp.
Cooper, E. L. 1976. Comparative
Immunology, Englewood Cliffs, N.J.: Prentice- Hall, 338 pp.
(Translated into Russian, 1980).
Wright, R. K. and Cooper, E. L.
(eds.) 1976. Phylogeny of Thymus and Bone Marrow-Bursa Cells.
Amsterdam, Elsevier/North Holland, 325 pp.
Gershwin, M. E. and Cooper, E. L.
(eds.) 1978. Animal Models of Comparative and Developmental
Aspects of Immunity and Disease. New York, Pergamon Press, 396
Cooper, E. L. 1982. General
Immunology. New York: Pergamon Press, New York, 343 pp.
Cooper, E. L. and Brazier, M. A.
B. (Eds.) 1982. Developmental Immunology: Clinical Problems and
Aging. UCLA Forum in Medical Sciences, Vol. 25, Academic Press,
New York, 321 pp.
Cooper, E. L. (Editor-in-Chief)
and van Miuswinkel, W. B. (Guest Editor) 1982. Immunology and
Immunization of Fish. Dev. Comp. Immunol. Suppl. 2: 255pp.
Cooper, E. L. and Wright, R.K.
(eds.) 1984. Aspects of Developmental and Comparative Immunology II.
Proc. 2nd Int. Congr. Int. Soc. of Dev. Comp. Immunol., Suppl.
3, New York, Pergamon Press, 280 pp.
Cooper, E. L., Langlet, C. and
Bierne, J., (eds.) 1987. Developmental and Comparative
Immunology, Alan R. Liss, N.Y., 180 pp.
Zapata, A. G. and Cooper, E L.
1990. The Immune System: Comparative Histophysiology.
Chichester , England: John Wiley & Sons, 334 pp.
Cooper, E. L. 1990. General
Immunology (Japanese Translation). Japan: Nishimura Co. Ltd., 324 pp.
Cooper, E. L. and Nisbet-Brown,
E., 1993. Developmental Immunology. New York: Oxford
University Press, 480 pp.
Vetvicka, V. Sima, P., Cooper, E.
L., Bilej, M. Roch, P. 1993. Immunology of Annelids. Boca
Raton, CRC Press, 300 pp.
Beck, G., Habicht, G.S., Cooper,
E.L. and Marchalonis, J.J. (eds.). 1994. Primordial Immunity,
Foundations for the Vertebrate Immune System. New York: New York
Academy of Sciences, 376 pp.
Cooper, E. L. 1996 (ed)
Invertebrate immune responses: Cells and Molecular Products. In: Adv.
Comp. Environ. Physiol. 23: 1-216.
Cooper, E. L. (ed.). 1996.
Invertebrate immune responses: Cell Activities and the Environment.
In: Adv. Comp. Environ. Physiol. 24: 1-249.
Beck G, Sugumaran M, and Cooper,
E.L. (eds). 2001. Phylogenic Perspectives on the Vertebrate
Immune System. Advances in Experimental Medicine and Biology vol.
484. New York: Kluwer Academic/Plenum Publishers 2001.
Cooper, E. L., Beschin, A. and
Bilej, M. A new model for analyzing antimicrobial peptides with
biomedical applications. Amsterdam, IOS Press 2002.
The Magic of Field Biology
Albert F. Bennett
Department of Ecology and Evolutionary Biology
University of California, Irvine
I was never a born biologist. I did not collect
insects, watch birds, or chase frogs. I was a rather bookish boy,
inclined more to remain indoors, rather than rambling around outside. I
liked reading about animals, but it was a more intellectual than
practical attraction. All that changed for me in college. While still a
sophomore, I began doing field work as a laboratory assistant for Bill
Mayhew at the University of California Riverside and spent a lot of
time camping in the desert. One morning I remember waking up at sunrise
and finding myself staring directly into the face of a kit fox, who
seemed less excited by the experience than I was. By the end of that
summer of noosing lizards and chasing snakes, I felt the transformative
magic of being with animals in their world. From that point, I knew my
calling and my career.
I have had the great fortune be able to undertake research expeditions
to study animals in the field in North, Central and South America,
Australia, and Africa. And it has been a privilege to be able to do
this in the accompaniment of great friends, mentors and colleagues. In
particular, my time in the field with my graduate advisor, Bill Dawson,
studying the thermal physiology of wallabies, birds, and lizards in
Australia was among the most rewarding and enjoyable experiences of my
Here I want to highlight just one of those expeditions. This was my
first trip to Africa. Ray Huey conceived and planned the expedition,
which included Ken Nagy, Henry John-Alder, and me. We went into the
Kalahari Desert, on the border between Botswana and the Republic of
South Africa, to compare the physiology, behavior, and energetics of
two closely-related species of lizards, one of which was a sit-and-wait
and the other, a widely-foraging predator. This was back in the good
old days, when two species comparisons without a phylogeny were still
considered respectable. We spent a month sweating through hot days,
watching animals daily and using doubly-labeled water to measure field
metabolic rates, energy intake, and water turnover. We converted our kitchen into a "controlled
temperature room" by turning the burners and oven on full blast and
regulated the temperature of our lizards in a "chamber" constructed of
a cardboard box and a hair dryer. We measured speed and endurance on an
ersatz racetrack and treadmill. You learn to improvise and invent and
make do, lemons become lemonade, and duct tape becomes the tool of
choice. It was challenging and fun, exhausting and incredibly
intellectually alive all at once. Part of my mind was always
concentrated on the data being collected. Bob Josephson once said that
as he collects data, he envisions how it will stand up to the
statistical analysis and how it will look in the published figures, and
I realized that is always how I worked as well: be sure that you have a
sufficient amount and then move on.
Looking back on that trip, however, it is not actually the
lizard study that draws my thoughts. More what I remember is just being
there in the field, in Africa. We had a memorable welcome to our field
site. I was walking the area looking for lizards, when a leopard
growled and jumped out of a bush not 50 meters from me. No gun, no run.
I was so dumbfounded that my first thought was to call out to Ray to
come over to see it. It snarled at me and then ran off. About 3 seconds
later the adrenalin hit, my heart nearly exploded, and my legs gave
out. Only then did I realize the danger; before that it was all wonder.
Later we saw the leopard often, with kills up in a tree. As we drove in
to work in the morning, we shared the road with brown hyenas going to
their den to sleep. Later we found their den, and in the late afternoon
would park by it and watch them play with their pups before going out
on a hunt. We saw an enormous mustard yellow cape cobra, nearly 2
meters long, climbing a tree to raid weaver finch nests. Lion were
common, including males with enormous black manes. At the edge of our
study site was a large acacia tree under which Ray had once seen a lion
with a kill on a previous trip. He told us about that just once too
often, and for the rest of the trip one of us would point out the tree
and tell the story to the others twice a day. There was a lot of that
kind of kidding and humor, and it helped to melt the frustration and
exhaustion associated the long hot days. We played a lot of music while
we worked. To this day I cannot listen to the Rolling Stones play Start
Me Up without going immediately back in my mind to the dry
bed of the Nassob River, where we listened to Tattoo You
as we watched ground squirrels using their tails as parasols to shade
themselves from the sun. My most enduring image of the trip is driving
back to camp at high speed late one afternoon, passing eland and
gemsbok, cheetah and lion, looking at enormous mauve thunderheads
blotting out the setting sun, promising rain that never arrived. What a
privilege it was to see that and be part of it, especially with such a
fine group of companions.
George Bartholomew once said that Africa is
special and pulls you in like no other place. That is certainly true
and part of what made this expedition so memorable. But part of it also
just being in a natural environment with animals living their own lives
outside of human needs and concerns. It is always magical to enter
their world and a privilege to be permitted to share it and to try to
understand in some small measure what it is like for them to live
there. As rules multiply and natural areas shrink and change, it is
more difficult to do, but it remains both rewarding and renewing.
B., A. F. Bennett, H. B. John-Alder, and K. A. Nagy. 1984. Locomotor
capacity and foraging behaviour of Kalahari lacertid lizards. Anim.
Behav. 32: 41-50.
A. F., R. B. Huey, and H. B. John Alder. 1984. Physiological correlates
of natural activity and locomotor capacity in two species of lacertid
lizards. J. comp. Physiol. 154: 113-118.
A., R. B. Huey, and A. F. Bennett. 1984. Field energetics and foraging
mode of Kalahari lacertid lizards. Ecology 65: 588-596.
A. F., R. B. Huey, H. B. John-Alder, and K. A. Nagy. 1984. The parasol
tail and thermoregulatory behavior of the cape ground squirrel (Xerus
inauris). Physiol. Zool. 57: 57-62.