SHORTPAPERS
467
Schellenberg, A. 1938. Litorale Amphipoden des tropischen Pazifiks. Kung\. Svenska Vetenskapakad. Hand\. ser. 3, 16: 1-105.
Sivaprakasm, T. E. 1968. A new species of Paranamixis Schellenberg (Crustacea: Amphipoda:
Anamixidae) from the Gulf of Manaar, India. Proc. Zoo\. Soc. Calcutta 21: 131-136.
Stebbing, T. R. R. 1897. Amphipods from the Copenhagen Museum and other sources. Trans. Linn.
Soc. London, 2nd ser. Zoo\. 2: 25-45.
--.
1906. Amphipoda I: Gammaridea. Das Tierreich 21: 1-806.
Thomas, J. D. 1979. Occurrence of the amphipod Leucothoides pottsi Shoemaker in the tunicate
Ecteinascidia turbinata Herdman from Big Pine Key, Florida. Crustaceana 37: 106-109.
Walker, A. O. 1904. Report on the Amphipoda collected by Professor Herdman, at Ceylon, in 1902.
Ceylon Pearl Oyster Fisheries. Supp\. Rep!. 1904, 17: 229-300.
DATE ACCEPTED: September 23, 1980.
ADDRESSES: (JDT) Newfound Harbor Marine Institute, Rt. 3, Box 170, Big Pine Key, Florida 33043;
(GWT) Department of Biological Sciences, Florida International University, Tamiami Campus,
Miami, Florida 33199.
BULLETINOF MARINESCIENCE.31(2): 467-470,
ANOMALOUS
1981
AERIAL ROOTS IN A VICENNIA GERMINANS
IN FLORIDA AND COSTA RICA
(L.) L.
Samuel C. Snedaker, Jorge A. Jimenez and Melvin S. Brown
A vicennia (Avicenniaceae) represents one of the dominant genera in the worldwide mangrove flora and the species are characterized by ascending, pencilshaped aerial pneumatophores (=pneumorhiza) which project vertically from the
sediment surface. Pneumatophores are negatively geotropic and develop as firstorder laterals (along with positively-geotropic descending anchoring roots) of
shallow, radiating horizontal roots (Jenik, 1978), also referred to as cable roots
in Chapman (1976). The pneumatophores have a nominal diameter of 8-10 mm
and a variable height ranging from a few centimeters to a reported maximum of
35 cm. They are further characterized by the presence of short absorbing rootlets
within the surface sediments and hydrophobic lenticels on the above-ground segment (see Chapman, 1976). Pneumatophores are the only form of aerial roots
known to be produced by A vicennia.
As a specific class of morphological adaptations, pneumatophores (also called
peg roots, knee roots, and root spines, depending on morphological variation)
occur among both halophytes and glycophytes in such diverse plant families as
the Pal mae , Taxodiaceae, Meliaceae, Rhizophoraceae, Combretaceae and Sonneratiaceae. It is generally agreed that pneumatophores are structural adaptations
which facilitate exchange of gases (oxygen and carbon dioxide) in anaerobic reducing environments typical of swamp habitats, and thus represent an example
of convergent evolution. For the halophytic mangroves, Chapman (1944) and
Scholander et al. (1955) provide experimental evidence for gas exchange which
occurs primarily through the lenticels but also via diffusion through the phelloderm. The related respiratory function of pneumatophores was experimentally
demonstrated by Chapman (1944) and more recently, demonstrated under field
conditions by Lugo et al (1975). Aerial prop or stilt roots in species of Rhizophora
(and Acanthus) have the same aerating function (see Scholander et aI., 1955;
Lugo et al., 1975; and Gill and Tomlinson, ]977) but are distinguished from pneu-
468
BULLETIN OF MARINE SCIENCE.
VOL. 31, NO.2,
1981
Figure l. (Left) Positively-geotropic aerial roots on the trunk of Avicennia germinans at an oil-spill
site in Tampa Bay. Florida. (Right) Negatively-geotropic, but deformed pneumatophores at the same
location.
matophores by having an above-ground origin and by exhibiting positive geotropic
growth (toward the ground). Statocysts have been identified in the aerial roots of
several mangrove species (Chapman, 1976) and thus geoperception is presumed
to be explained by the statolith hypothesis (Juniper, 1976).
Recently, we observed anomalous, positively geotropic aerial roots on the
trunks of A vicennia germinans (L.) L. in both Florida (Fig. I left) and Costa Rica
(Figs. 2 left, right). Also, at the Florida site we observed an aberrant morphological development of pneumatophores (Fig. 1 right). Anomalous aerial roots
and pneumatophores of these types, heretofore, have not been reported in the
literature.
The anomalous aerial roots and aberrant pneumatophores in the Florida A.
germinans were observed along the eastern shore of Tampa Bay approximately
2 years following the S.S. Howard Star oil spill. That spill, on 5 October 1978,
consisted of some 40,000 gallons of bunker C, lubricating oil and "slop" tank
petroleum fractions which impacted portions of a mangrove-dominated shoreline.
In one affected area, approximately 1.1 ha in size, 27% of the Rhizophora mangle
L. and 39% of the A. germinans died within 2 years of the spill event (Getter et
al., 1980). Some individuals of A. germinans which survived the initial impact
subsequently lost an unknown number of their pneumatophore complement, presumably due to suffocation and/or chemical toxicity. At the time photographs
(Figs. 1 left, right) were taken on 17 January 1980, we observed apparently-normal
pneumatophores on un-oiled substrates and decomposing pneumatophores on
portions of the substrate retaining oil residues. In addition, we observed anomalous descending aerial roots on lower trunks and the regeneration of both normal
and aberrant pneumatophores. One tree (Fig. 1 left) which appeared to have lost
the majority of the pre-spill pneumatophores exhibited growth of descending aerial roots on the lower trunk. We could not determine in the field if these descending aerial roots were anatomically analogous to cable roots or first-order
laterals, i.e., pneumatophores or anchoring roots, or some other structure. The
gross morphology of these structures was similar to that of normal pneumatophores except for relatively large diameters (11-13 mm). The regenerating pneumatophores of the tree in Figure 1 right exhibited negative geotropic growth but
SHORT PAPERS
469
Figure 2. (Left) Positively-geotropic aerial roots on the trunk of Avicennia germinans near Moin,
Costa Rica. (Right) A second example of anomalous aerial roots at the same location.
several were unusually long and twisted. We believe that the appearance of these
anomalous aerial roots and aberrant pneumatophores is a response to a chronic,
sublethal stress in the rhizosphere, an associated loss of the normal complement
of surface pneumatophores, and an inability to regenerate new pneumatophores
in portions of the sediment that remain toxic. The phenomena of both positive
geotropic development and aberrant twisting suggest, respectively, an induced
reversal in geoperception and defective statoliths which are only partially and/or
intermittently active.
The anomalous aerial roots in Costa Rica were observed during the summer of
1980 in the vicinity of Moin on the Atlantic coast. Photographs (Figs. 2 left, right)
were taken of several trees from a small, localized population exhibiting the
phenomenon. There was no evidence of any pollutant impact as in the Florida
example; however, within the immediate area of affected trees there was an
intense odor of hydrogen sulfide following disturbance of the substrate. This area
around Moin is perpetually wet (annual precipitation, 3,800 mm/yr) and during
most of the year is inundated with freshwater. The low salinity of this environment permits the forest dominance to be shared by the transitional halophyte,
Pterocarpus officinalis Jacq., and glycophytes represented by the genera Hyrnenocallis, Pancratiurn and Montrichardia (Pool et al., 1977, for a structural
description of the forest). The humid conditions are also reflected in the abundance of epiphytes on the trunks of the trees and in the canopy which is an
atypical situation in a pure halophytic mangrove forest (Jimenez, in prep.). The
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BULLETINOF MARINESCIENCE.VOL.31. NO.2. 1981
descending aerial roots on A. germinans ranged up to 30 cm in length and grew
from the trunks to a height of 3.5 m above ground level. We believe that in this
situation the anomalous aerial roots have been induced by prolonged flooding and
a small area of an anoxic, intensely reducing substrate. The subcanopy humidity,
which is normally high in this area, may facilitate the growth of the anomalous
aerial roots to considerable heights on the trunks.
Although the mechanisms which induce the formation of anomalous aerial roots
are unknown, these observations suggest that the effects are a response to toxic
substrates (e.g., petroleum residues, anoxia and hydrogen sulfide) which limit the
normal functioning of pneumatophores. The ability of A. germinans to develop
anomalous aerial roots on above-ground trunks and regenerate pneumatophores
following a stress may permit the continued survival of the tree in an altered or
otherwise unfavorable habitat. The existence of these anomalous aerial roots also
demonstrates an unusual degree of morphoplasticity in these structures.
ACKNOWLEDGMENTS
Funds for the Florida research were provided by the Florida Department of Natural Resources and
for the Costa Rican research by the Consejo Nacional de Investigaciones Cientificas y Tecnologicas
and the Rosenstiel School of Marine and Atmospheric Science. We thank J. Fell, G. Voss and two
anonymous reviewers for helpful suggestions with an earlier version of the manuscript. J. Snedaker
typed the final manuscript.
LITERATURE
CITED
Chapman, V. J. 1944. 1939 Cambridge University expedition to Jamaica. J. Linn. Soc. Bot. 52: 407533.
--.
1976. Mangrove vegetation. J. Cramer, Leutershausen. 499 pp.
Getter, C. D., S. C. Snedaker and M. S. Brown. 1980. Assessment of biological damages at the
Howard Star oil spill site, Hillsborough Bay and Tampa Bay, Florida. Report to the Fla. Dept.
Nat. Res., Tallahassee. 65 pp.
Gill, A. M., and P. B. Tomlinson. 1977. Studies on the growth of red mangrove (Rhizophora mangle
L.). 4. The adult root system. Biotropica 9: 145-155.
Jenik, Jan. 1978. Root and root systems in tropical trees: morphologic and geologic aspects. Pages
323-349 in P. B. Tomlinson and M. H. Zimmermann, eds. Tropical trees as living systems.
Cambridge Univ. Press, N.Y. 675 pp.
Juniper, B. E. 1976. Geotropism. Ann. Rev. Plant. Physio\. 27: 385-406.
Lugo, A. E., G. Evink, M. M. Brinson, A. Broce, and S. C. Snedaker. 1975. Diurnal rates of
photosynthesis, respiration and transpiration in mangrove forests of south Florida. Pages 335350 in F. B. Golley and E. Medina, eds. Tropical ecological systems, ecological studies, Vo\. II.
Springer-Verlag, N.Y. 398 pp.
Pool, D. J., S. C. Snedaker, and A. E. Lugo. 1977. Structure of mangrove forests in Florida, Puerto
Rico, Mexico, and Costa Rica. Biotropica 9: 195-212.
Scholander, P. F., L. van Dam, and S. I. Scholander. 1955. Gas exchange in the roots of mangroves.
Amer. J. Bot. 42: 92-98.
DATE ACCEPTED: November 26, 1980.
ADDRESSES: Division of Biology and Living Resources, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149.