FOUNDATIONS OF GREGARIOUSNESS IN BARNACLES
University of Hawaii at Manoa
toonen{at}hawaii.edu
Robert J. Toonen writes about E. W. Knight-Jones' classic 1953 publication on gregariousness during settling in barnacles.
One of the major thrusts of marine biologists through the 1950s and into
the 1960s was to examine the role of settlement behavior of planktonic larvae
in contributing to the distribution and abundance of adult marine
invertebrates. This effort was the birth of both supply-side ecology and the
first attempts to isolate and characterize the specific substratum-bound
substances to which larvae respond at the time of settlement. E. W.
Knight-Jones was among the leaders in this area, along with a handful of
others (reviewed by Young,
1990), and his work continues to be widely emulated and expanded
upon by researchers in the field of larval ecology today. A literature survey
by Pechenik et al. (2001
)
indicates that relatively few papers continue to be cited more than 50 years
after they are published, and fewer still are cited more often now than when
they were first published. E. W. Knight-Jones'
(1953
) article published in the
Journal of Experimental Biology is among those exceptions that
continue to be widely cited in the modern literature. In fact, this paper has
been cited 196 times since 1990, and nearly a half-century after publication
this paper continues to be cited in such prominent journals as Proceedings
of the Royal Society of London Series B, Ecological Monographs, Ecology,
Oecologia, Evolution, Peptides, Aquatic Microbial Ecology and Marine
Ecology Progress Series.
Knight-Jones' paper sought to understand the role of settling behavior of
larval barnacles on establishing the aggregated distribution of adults.
Approximately 80% of marine organisms (about 90,000 species), both vertebrate
and invertebrate, have a biphasic life-cycle and produce planktonic larvae,
which spend some variable amount of time (ranging from minutes to months)
developing in the water column before settling and metamorphosing into the
adult life-form (Thorson,
1950). The choice of settlement site is important because the
animal will remain here for the rest of its adult life. Knight-Jones tested
the attractiveness of a variety of substrates to larval barnacles at the time
of settlement. Through a series of laboratory settlement assays, he
established that barnacle larvae recognize cues specifically associated with
adult barnacles, are attracted to these cues, and therefore settle near
conspecifics. Further, this paper was among the first to attempt to
characterize the chemical nature of a settlement cue or metamorphic inducer
for the larvae of marine invertebrates (for a recent review, see
Pawlik, 1992
). Knight-Jones'
paper presented only qualitative observations of settlement preferences.
However, his results are generally sufficiently striking that the absence of
statistics does not impede interpretation of the results, and this paper
remains among the more thorough of single papers on the settling behavior and
nature of the settlement cue for any marine organism published to date. The
paper is most widely cited for two different aspects: (1) it presents
convincing evidence that larval barnacles are gregarious and active in their
settlement choices, and (2) it reveals that the contact-dependent cue to which
larvae respond appears to be a cuticular protein. However, there are many
additional nuggets in this paper that continue to make it a worthwhile read
for larval biologists today.
Knight-Jones showed, for example, that cyprid larvae, the specialized stage
of barnacle larval development that is competent to settle, are capable of
prolonging their planktonic lives and delaying metamorphosis into juveniles.
The capacity to delay metamorphosis is considered adaptive because it
increases the likelihood of locating suitable habitats and may promote genetic
exchange among populations (reviewed by
Pechenik, 1990). Knight-Jones'
paper was certainly not the first to document a capacity for competent larvae
to delay metamorphosis, but it was one of the early papers that document a
cost to that delay. Although Knight-Jones attributed the cost solely to larval
encumbrance by bacterial growth, he documented that juveniles from delayed
settlers were capable of metamorphosing at a reduced size, and that larvae
which delayed by more than 2 weeks became sluggish and were frequently unable
to settle.
The paper also presented one of the first comprehensive surveys of
potential settlement cues and experimental treatments to determine the
chemical nature of the substratum-derived cue (reviewed by
Rittschof and Cohen, 2004).
Through serial exposure of the putative cue (the bases of conspecific
barnacles) to heat, solvents, acids and alkalis, oxidizing agents and,
finally, reagents that react with proteins, Knight-Jones concluded that the
cue was most likely a quinone-tanned protein from the epicuticle of settled
barnacles (for a recent review, see Clare
and Matsumura, 2000
). He went on to demonstrate that settlement in
response to conspecific barnacles was highest, but response to other species
of barnacles was still higher than settlement on uninhabited surfaces (also
reported by several recent workers, such as
Matsumura et al., 2000
).
Knight-Jones also points out that secondary cues (additional cues beyond
simply the presence of the epicuticular protein) are important to barnacle
recruitment decisions because larvae `sensitized' by physical contact with
conspecifics would settle on nearby uninhabited rough granite rather than
smooth glass surfaces inhabited by barnacles. The potential disadvantage of
attaching to a perfectly smooth surface, such as plate glass, is obvious for
an organism living in the pounding surf. The specific ranking of settlement
cues used by barnacle larvae was later explored in detail by Wethey
(1986
).
Finally, there is an observation, mentioned several times in Knight-Jones'
paper, that "isolated bare surfaces collect abnormally
undiscriminating pioneer settlers, which are soon followed by gregarious
individuals." This observation, apparently viewed as an aberrant
behavior by Knight-Jones, was later followed up in a number of papers (e.g.
Krug, 2001;
Toonen and Pawlik, 1994
) that
documented similar behavior among the larvae of other species, and argue that
this strategy is a form of bet-hedging (reducing the risk of reproductive
failure by distributing offspring among a variety of habitats) or a dispersal
polymorphism (production of two or more larval types with differential
proclivity to disperse and settle). Such variation in settlement preferences
among individual larvae should increase individual fitness for marine
invertebrates with planktonic larvae (reviewed by
Toonen and Pawlik, 2001
).
Knight-Jones argued that the level of discrimination shown during larval
settlement should be subject to individual variation, an idea that was largely
lost to the field until rekindled by Raimondi and Keough
(1990
), and later demonstrated
experimentally (e.g. Gibson,
1995
; Krug, 2001
;
Toonen and Pawlik, 1994
).
With the volume of publications today, no one can read all the papers
coming out each year in any particular field. Researchers are routinely
turning to electronic databases to search the massive volume of literature in
their field, but even the best of these databases contain only about 30 years
of citations. Given the ease with which it is possible to search electronic
databases today, it is not surprising that relatively few of the papers
published before the age of computers are commonly cited in the current
literature (Pechenik et al.,
2001). Thus, I applaud the concept of the JEB Classics, and am
honored to be part of the effort to reintroduce classic papers from before the
age of PDFs into the electronic databases of today. E. W. Knight-Jones'
classic JEB paper has provided a great deal of inspiration for researchers in
the field of larval ecology, and continues to be cited widely today. It was a
pivotal paper in formulating my early research interests, and I hope that
making it easily accessible to future generations of larval biologists will
continue to provide similar stimulation.
This is contribution #1193 from the Hawaii Institute of Marine Biology and SOEST #6544.
Footnotes
A PDF file of the original paper can be accessed online: http://jeb.biologists.org/cgi/content/full/208/10/1773/DC1
References
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