Chapter thirteen
Sources of plasticity in
behavior and its
physiology: sex, hormones,
environment and the
captivity model
Robert E. Landsman
13.1 COMMENTS ON
BEHAVIORAL PLASTICITY
Behavioral plasticity (or variability) is the
rule, not the exception, and in many instances, environmental perturbations are
a major cause of variability observed in behavior. To the extent that changes
or differences in environmental conditions persist, differences in response
between and/or within members of a single species will persist in both field
and laboratory. Consequently, the scientist who employs behavior as an end
point in his/ her research must carefully assess alternative hypotheses to
explain variability in results, and sometimes the elimination of outliers may
be the elimination of the most valuable findings. Serendipity does not just
occur, it is ferreted out by the reflective investigator.
The
electric organ discharge (EOD) is highly variable, its waveform and frequency
(or rate) being at the mercy of a number of parameters. Certain characteristics
of the EOD are sex and hormone‑dependent and are affected by
maturational, developmental (Chapter 12) and a host of incidental, environmental
factors (e.g. seasons, water quality, captivity). Variability in the EOD even
results from distortion caused by objects close to the fish's body surface,
providing the cues for active electrolocation
(Chapters 5, 17).
304 Sex,
hormones, environment and the captivity model
The variability observed in the EOD emitted by
both the African mormyrids and the South American gymnotiforms is an excellent
indicator of fluctua-tions in these fish's aquatic
habitat and should be considered as a prime example of plasticity and tire
expression of individual variation in a behavior.
This
chapter will focus on the topic of variability in the EOD of weakly electric
fish resulting from factors such as sex, endocrine status, and environmental
perturbations. I will present a rather critical view of the current state of
this field by examining findings, dilemmas, contradictions, and possible resolutions
presented by published data.
Throughout
this chapter, I will use the following abbreviations denoting various hormones:
T (testosterone), DHT (dihydrotestosterone), 11‑KT
(11-ketotestosterone), 17MT (17α‑methyltestosterone, E2
(estradiol), and the steroid hormone precursor CHOL
(cholesterol). Measures of the individual EOD will be referred to as the
duration and/or amplitude of the individual phases of the EOD (P1, P2, P3 and P4), and
the peak power spectrum frequency (PPSF) of the fast Fourier transform
associated with the EOD. As a rule, the shorter the individual EOD, the higher
the PPSF; and conversely, the longer the EOD, the lower the PPSF. However, an
increase or decrease in PPSF may result from changes in the durations of only
specific phases of the EOD: statistically, the PPSF is also more related to the
duration of some phases than to others (Landsman, 1993a,b). Measures of the
rate or pattern of EODs will be referred to as SPIs (Chapter 8).
13.2 SEX‑RELATED
AND HORMONALLY INDUCED EOD
PLASTICITY
Sex differences in EODs have been reported for
both South American gym-notiform and African mormyrid
species. Because the EOD is sensitive to
gonadal hormones, sex‑typical
EODs can be reversed to resemble those of
the opposite sex by gonadal
manipulation and steroid hormone adminis-tration, and
sex differences are highly correlated with season, gonadal maturity
and reproductive state. Generally, the studies that suggest EOD sex
differences were performed in the field, employed small samples, and are
comprised largely of descriptive. non‑statistical accounts of natural sex
dif- ferences in EOD waveform, duration, arid/or SPIs
for several gymnotiform and mormyrid species. These field‑reported sex
differences have rarely been reported in laboratory studies, and if so, only
anecdotally or in one or two species
which were bred in the laboratory. But both laboratory studies (reviews: Meyer, 1983; Bass and Hopkins, 1985;
Meyer et al., 1987;
Mills and Zakon, 1987 Landsman et al., 1990:)
and field studies (Bass and Hopkins, 1983, 1985: Hagedorn and Carr,
1985) have employed hormone
Sex‑related
and hormonally‑induced EOD plasticity 305 305
manipulations to induce male‑ or female‑like
EODs. The majority of the field studies reporting sex differences show
considerable variability and overlap between the sexes. The majority of studies
involving hormone manipulation lack important control groups (i.e. CHOL.‑treated
fish to control for the effects of non‑gonadal steroid hormones, fish
administered blank implants to control for the effects of steroid hormones and
CHOL implants and nonhandled fish to control for the
effects of' all handling including surgical manipulations), and/or many include
control groups of small sample size (e.g. n = 3) composed of both sexes and/or
mixtures of juveniles and adults of both sexes. In many cases, studies used
only methylated androgen, which does not naturally
occur in fish, or DHT, which does not appear to be a major androgen in fish
(although in the guppy, Poecilia
reticulata,
the ability of follicles to synthesize 5 α‑DHT in vitro from
precursors has been demonstrated by Venkatesh et al.,
1991).
Endocrine
studies on weakly electric fish commonly employ the methyl- lated androgen, 17‑MT
(Bass and Hopkins, 1983, 1984; Bass, 1986a;
Landsman and Moller, 1988) which
is more potent than T. Although MT may be used to induce male‑typical
behavior in many fish species, the effects of this hormone are exaggerated and
may be pharmacological in nature. especially when compared with the
effects of T. Landsman and Moller (1988)
implanted MT into juvenile and adult Gnathonemus
petersii and found up to a fivefold
increase in total EOD duration accompanied by large decreases in PPSF from 4100
to 400 Hz! In contrast, Landsman et al. (1990) employed T implants resulting in
plasma levels of T in the range found in
breeding males, and resulting in total EOD duration increases of up
to 33%) with smaller decreases in PPSF to above I kHz (see also Fig. 13.11 ). Problems of hormone dose are
compounded when the effects of MT are
compared with the effects of non‑methylated DHT
or E2 (e.g. Bass and Hopkins, 1983, 1984; Bass, 1986a). Thus, one
must be careful in the interpretation of results obtained with MT
unless substantiated with T or 11- KT, the two predominant androgens found in
fish. DHT was found to be less potent than T in producing behavioral effects on
the EOD, and did not have any effects on PI and P4 in juvenile Gnathonemus petersii (Landsman et al.,
1990). However, the differences in DHT and T may be a dose effect since DHT has
been shown to clear more rapidly than an equivalent dose of T
in other species (discussion: Harding, 1986). Further, many studies on electric fish employed different procedures
for the administration of hormones. including injections, pellet implants
and time‑released silastic implants. Many of the above factors have added
to the variability in findings on sex differences in and hormonal
control of EOD behavior, and have made it particularly difficult to make
generalizations regarding the sensitivity of the EOD to steroid hormones as
well as to make comparisons of steroid effects across and within studies
and species.
306 Sex, hormones, environment and
the captivity model
The
remainder of section 13.2 will focus on those species in which there appears to
be sufficient complementary data to warrant the claim for the existence of sex‑related
EOD differences and their sensitivity to steroid hormones. (When data based on
small samples are cited, the number of subjects is provided.) However, except
for one mormyrid species, Gnathonemus
petersii, the differences between the sexes are overlapping and in many
cases ambiguous: thus, the term 'sexual dimorphism' will not be used to
describe these sex‑related EOD characteristics.
Gymnotiformes
Some gymnotiforms exhibit a sex difference in
their EOD waveform and/or frequency (Chapters 8, 12, 18). Mature female Sternopygus macrurus discharge at higher
frequencies than mature males, while juveniles discharge at frequencies
intermediate between the two (Hopkins, 1972, 1974a; Zakon et al., 1991b; Mills et al., 1992).
When intact S. macrurus were
implanted with silastic capsules containing DHT, the EOD rate decreased and EOD
duration increased significantly compared with both pre‑implant values
and EODs of controls implanted with blanks (Mills and Zakon, 1987: Mills et al., 1992). Two of the authors'
controls, however, also appeared to show consistent changes in EOD frequency
and duration over the experimental period, but in directions opposite to each
other (shown in Mills and Zakon, 1987, figs. 8(b) and 10(b), respectively).
Whether these data reflect effects of the implants themselves is difficult to
interpret as this study did not include a non‑implanted control group. Removal
of the DHT implants from three subjects for 63
days resulted in EOD rates and durations comparable to pre‑implant
values, while three fish with sham removal of' DHT implants retained their
lowest EOD rates and longest durations, suggesting that the steroid effects on
the EOD are not permanent in this species.
A field
study, in which EOD data were recorded and blood samples obtained from the same fish, indicated sex‑specific
relationships between EOD frequency and endogenous steroid levels in S. macrurus
which sug- gested that
androgens, but not E2, modulate EOD frequency in this species (Zakon
et al., 1991b). Males exhibited lower
EOD rates than females, and plasma levels of T and 11‑KT, but not E2,
were inversely related to EOD rate in males, while plasma levels of T and E2
in females were not related to FOD rate (Zakon et al., 1991 b). Interestingly, the EOD sex difference in this
species wits maintained across seasons over which T levels varied in both males
and females, even though males with low levels of androgens had a wide range of
EOD frequencies (Zakon et al., 1991b).
This suggests that (1) the male EOD may be influenced by factors other than
androgen when T and 11‑KT
levels are low (Zakon et al., 1991 b), and (2) the sex difference in
Sex‑related
and hormonally‑induced EOD plasticity 307
EOD characteristics in
this species is maintained by unknown factors in addition to androgen.
Female Sternopygus
dariensis also emit higher EOD rates than males (Meyer,
1983; Chapter 12). Meyer (1983) injected males and females with T, DHT, or E2 in various doses
ranging from 2.5 to 20.0 µg/g body weight.
Following androgen injections, both sexes lowered their EOD rates. Fish with higher pre‑treatment frequencies
showed larger responses to the hormone
treatment than fish discharging at lower frequencies. Unlike S. macrurus, fish treated with E2 showed
frequency effects in the opposite direction
to those treated with androgen.
Further, castrated males showed an 11%
increase and ovariectormized females an 18%) decrease
in EOD rate. Hormone replacement reversed the effects of the surgery, while adminis-tering heterologous
hormones to either sex increased the effects of gonadectomy.
Thus, hormonal effects on the EOD rate of S.
dariensis are not permanent, but rather are activational in
nature. This means that the electric
organ in this species may be bipotential in its
ability to emit male- or female‑like
EODs, and it is likely that the presence or absence of gonadal hormones in adulthood
determines the sexual characteristics of the EOD.
Eigenniannia
virescens (E. lineata: Chapter 18) exhibits a sex difference in EOD rate in the
same direction as Sternopygus (mature
females possess a higher EOD rate than males) but with much overlap between the
sexes (
tures fell within a wide
range of intermediate frequencies. As the fish became ripe, females shifted their
frequency in the upward direction and in many cases surpassed the males' rates
(Westby and Kirschbaum, 1981), suggesting
hormonal involvement in the EOD rate of this species. These incongruent findings suggest at least
three possible explanations: (1) some
of Hopkins' (1974b) fish were gonadally ripe
and producing hormones that influenced EOD rate, (2) the EOD rate is sensitive
to seasonal changes in reproductive
state (page 323), and/or (3) the EIOD rate is affected by cap-tivity (page 336). Sex differences have also been reported
in the waveform and harmonic content of Eigenmannia
EOD activity, with males having a lower ratio of head‑positive to
head‑negative EOD phase durations and a higher content of higher
harmonics (Fig. 13.1; Westby and Kirschbaum,
1981; Kramer, 1985; Kramer and Otto, 1988). The sensitivity of the EOD to steroid hormones has not been adequately studied in this
species to make
any conclusions
regarding the hormone dependence of the sex difference(s), although androgen
injections purportedly decreased the EOD rate (unpubl.
data, cited in Meyer et al., 1987).
Compared with females, mature male Brachyhypopomus occidentalis (formerly Hypopomus) ( a pulse‑type gymnotiform ) have broader tails
308 Sex, hormones, environment and the captivity model
Fig. 13.1 Fourier amplitude spectra (left) and
EODs (right) of female (A) and male (B) Eigenmannia lineata. Notice the lower
ratio of positive to negative EOD phase durations (the identical EOD
frequencies in both sexes seem to be coincidental), and the higher content of
higher harmonics in the male's EOD compared with the female's signal. Zero
potential level is indicated by dotted horizontal line. Modified after Kramer
and Otto (1988).
containing electric organs with larger
electrocytes that produce EODs with smaller PI/112 duration ratios and lower
PPSFs (Hagedorn and Carr, 1985). If the size of the electrocytes accounts for
both tail size and EOD sex differences, then it is not surprising that male
PPSFs were significantly negatively related and female PPSFs positively related
to tail width (Hagedorn and Carr, 1985) (see 'Notes on membrane effects', page
323). When females were injected with 5 pg/g of either DHT or E2,
DHT‑treated fish developed larger, male‑like electrocytes along
with male‑like EODs that were characterized by a significant increase in
the duration of P2 and a 71% decrease in PPSF, while E2‑treated
fish showed no change in electrocytes or EOD (Hagedorn and Carr, 1985).
Mature
female Apteronotus (a gymnotiform with a neurogenic electric organ; Chapters 8,
18) spawned and raised in the laboratory exhibit lower EOD rates than males,
i.e. a sex difference opposite in direction to that shown
in other gymnotiform species, although considerable overlap between the sexes has been reported
(Kirschbaum, 1983; Hagedorn and Heiligenberg, 1985; Meyer et al., 1987). Silastic implants containing estrogen (E2), but not those
containing androgen (DHT), decreased the EOD rate as compared with blank
implant controls (Meyer et al.,
1987). Since non‑handled and CHOL‑implanted controls were not
included, and since all implants
contained less than
0.5 mg of steroid
and the actual dose
Sex‑related
and hormonally‑induced EOD plasticity 309
administered to each
subject is unclear, a more detailed study is needed to make conclusive
statements about the hormonal dependence of the EOD in this species.
Interestingly, Meyer (1984) injected E2, T, α‑ or β‑DHT,
or saline and reported temporary androgen‑induced
in vivo EOD frequency decreases, and in vitro decreases in pacemaker
activity, and no E2 effects. These findings appear to demonstrate
that short‑term EOD hormone sensitivity in this species is due to direct
action of the hormones on the pacemaker. However, saline injection caused both
significant short‑term decreases and increases, and longer‑term
decreases in EOD frequency, although these decreases were significantly smaller
than those caused by androgens. Because injections of saline also influenced
frequency, an accurate interpretation of the steroid data would necessitate a
non‑handled control group, carried through the course of the study,
and/or baseline data collected on the same subjects prior to beginning of the
injection regime for statistical comparison. Also, because EOD data were only
collected over the 7 day injection period, it is difficult to draw conclusions
about long‑term post‑injection hormone effects.
Mormyridae
In their natural habitats, but also on a few
occasions in laboratory‑bred specimens, several mormyrid species appear
to exhibit sex differences that are reflected in temporal (duration) and/or
spectral features (PPSF) of the individual EOD, and sometimes expressed in the
sequence of pulse intervals (SPIs) (Chapters 8 and 12; review: Zakon, 1993).
EODs are steroid sensitive, and so these sex differences can be altered through
administration of steroid hormones in all species investigated (reviews: Bass,
1986a; Landsman et al., 1990;
Landsman, 1993b: Zakon, 1993: Landsman and Moller, in prep). In mormyrids, EOD‑related
sex differences found in the field are elusive under laboratory conditions.
Field studies have indicated that Brienomyrus
brachyistius (long biphasic) (Bass and Hopkins, 1983), Brienomyrus brachyistius (triphasic)
(Bass and Hopkins, 1983, 1985), and possibly Stomatorhinus corneti (Hopkins, 1980; Bass and Hopkins, 1985), S. walkeri (Moller, 1980: Fig. 8.9 (13)) and Hippopotamyrus batesii (triphasic) (one
male and two females: Bass and Hopkins, 1985) may all exhibit sex differences
in EOD waveform and/or duration. Males typically emit EODs that are two to
three times longer (and thus exhibit lower PPSFs) than those of females
(Moller, 1980; Hopkins, 1980, 1981a; Hopkins and Bass, 1981; Bass and Hopkins,
1983, 1985).
The
species identification of Brienomyrus is not
clear. Following the con-vention established in
Chapter 8 (Fig. 8.11), fish studied on location or imported from
310 Sex, hormones, environment and the captivity model
sites in
Although
EOD sex differences have yet to be fully substantiated, the following species
all have steroid‑sensitive EODs: Brienomyrus
sp. and Brienomyrus sp. 2 (Bass
and Hopkins, 1984, 1985; Bass, 1986b; Bass and Volman, 1987), Campylomormyrus tamandua and Hyperopisus bebe (n = 1 fish of each
species; Bass, 1986b), and Stomatorhinus
corneti and Hippopotamyrus batesii (one
fish treated with MT and one with T propionate, respectively) (Bass and
Hopkins, 1985).
The
following subsections contain a more detailed discussion regarding EOD‑related
sex differences and steroid effects in these species as well as in Gnathonemus petersii with an EOD‑related
sexual dimorphism demonstrated in the laboratory.
Brienomyrus brachyistius
(long biphasic) (
Male B.
brachyistius (long biphasic) exhibit
EODs of longer duration with lower PPSFs and different waveforms than females
(Bass and Hopkins, 1983). 17‑MT added to the water induced male‑like
EODs in intact (adult females, and in one juvenile male and female) or
gonadectomized fish (one juvenile male and female, and one adult female) by
increasing the EOD duration twofold with decreases in PPSFs (Fig. 13.2).
Androgen‑induced
effects on the EOD in this species appear to be temporary as the EODs of the
intact androgen‑treated fish reverted to the female type EOD over 24 days
after treatment was terminated by placing the fish in fresh water (Bass and
Hopkins, 1983). Intact (two juvenile males and one adult female) and one
gonadectomized fish implanted with DHT pellets also exhibited male‑like
EODs, while E2 had slight effects on the EOD of immature fish (males
and one female) (Bass and Hopkins, 1983). Surprisingly, E2 treatment
also resulted in a downshift in PPSF and an increase in EOD duration; however,
these changes were not as dramatic as those resulting from androgen treatment
(Bass and Hopkins, 1983). Thus, it is possible that E2 exerts only a
partial masculinizing effect on the EOD because estrogen receptors might not
yet be developed or functional in juvenile fish.
These
findings implicated androgen as a mediator of maleness in the mormyrid EOD, and
suggest that E2 does not have a complete activational, masculinizing
influence on the female EOD. Because DHT cannot be con-verted
to E2 by way of aromatase activity, and because E2 has
some mas-culinizing effects, the extent to which androgen is solely responsible for the
Sex‑related
and hormonally‑induced EOD plasticity 311
Fig. 13.2 Time course of changes in EOD duration
during hormone treatment periods in Brienornyrus
brachyistius (long biphasic); representative EODs are shown, each symbol is for
one individual. The stippled area to the left of all but one plot is the range
of EOD duration for immature and female fish for one standard deviation (0.161
ms) to either side of the population mean (0.908 ms, n = 25). Dashed lines
represent a least‑squares fit to the straight line (CTL, E) or an
exponential curve (17MT, post 17‑MT, GonadX +
17-MT, DHT). Changes in EOD duration were non‑significant for the non‑treated
control (CTL) and estradiol (E) pellet‑implanted
subjects; but significant when powdered testosterone was added to intact (17‑MT)
or gonadectomized (GonadX + I 7‑MT) fish, and
after it was removed (post I 7‑MT). Thin arrows point to individuals from
which EODs were recorded. Modified after Bass and Hopkins (1983).
expression of
maleness in the EOD of this species is not yet clear. The effect
of CHOL
on the EOD of B. brachyistius (long
biphasic) has not been investi-
gated (compare Bass and Hopkins, 1983, with Bass
and Hopkins, 1985: p. 601).
312 Sex, hormones, environment and the captivity model
Androgen‑specific
receptors have been found in the electric organs of adult mate B. brachyistius
(long biphasic), and a possible sex difference in binding activity was
suggested by preliminary data (Bass et
al., 1984). However, additional assays failed to confirm this result (Bass et al., 1986b). Because a sex difference in androgen binding to receptors in the
cytosol of efectrocytes
could account for sex differences in the EOD waveform, more work in this area
needs to be performed on other mormyrid species. Further, Bass et al. (1986b), using autoradiography,
found 3H‑DHT binding cells in the brain adjacent to the relay
cells of the medullary command nucleus. (These cells
project to the spinal motor neurons that innervate the electrocytes of the
electric organ; Chapter 16.)
Brienomyrus brachyistius
(triphasic) (
The E0D of B.
brachyistius (triphasic)
exhibits sex differences in waveform and duration (Hopkins and Bass, 1981; Bass and Hopkins, 1985). The sexually mature male EOD is
usually double in duration with lower PPSFs and of distinctly different shape
from that of females or juveniles (Fig. 13.3 (A)). However, maleness of the FOD
varies with the size of the fish, and the EOD of large adult females overlaps
with those of males (Bass and Hopkins, 1985).
Bass
and Hopkins (1984) reported that both
androgens, 17‑MT and DHT, induced male‑like EODs in females and
juveniles, expressed in increased duration and decreased PPSFs (Fig. 13.3 (B)).
Surprisingly, E2 pellet implants or injections also increased EOD
duration, lowered peak power, and induced the male‑like waveform shape
(Bass and Hopkins, 1985). B. brachyistius
(triphasic) has not been subjected to treatment
with CHOL or blank implants; it is thus difficult to assess the extent to which
the EOD changes were due to surgery, implants, or general or specific hormone
effects.
Interestingly,
when five fish treated with 17‑MT, dissolved in water, were placed in
fresh water for 25 days, their
hormone‑induced male‑like EODs did not completely revert to pre‑treatment
forms, suggesting that the effects of androgen on the EOD in this species may
be relatively permanent (Bass and Hopkins, 1985). The authors claimed that this permanence is also supported by: ( 1
) the EOD of mature males maintained in captivity for 3 months (n = 3) or 6
months (n = 1) did not revert to the female form (however, only the final day's
EOD is presented; fig. 8 in Bass and
Hopkins, 1985); (2) one transitional male became more male‑like,
and one female with a male‑like EOD (Fig. 13.3) became more female‑like
in captivity: and (3), when one mature male was castrated, its EOD remained
unchanged (male‑like).
Sex‑related
and hormonally‑induced EOD plasticity 313
Fig. 13.3 (A) Oscilloscope tracings of EODs from Brienomyrus brachyistius (triphasic) recorded in the field. Notice the differences in
shape and duration between female/ juvenile
(n = 9) and male EODs (n = 3). (B)
EODs of several individuals of B. bra- chyistius (triphasic): juveniles treated with 17α-methyltestostcrone
(juvenile/testos- terone) or 5α‑dihydrotestosterone
(juvenile/DHT) show a change in EOD duration
over 10 days (10d). The EOD duration of a
captive male with a 'transitional' waveform (transitional male)
becomes more male‑like in captivity (6d, 12d). In contrast to all of the above, the
EOD waveform of captive females (female/control) or juveniles (juvenile/control)
remains unchanged when kept in captivity for compare- able times. Interestingly, the
transitional male appears to be more female-like than the female control on 0d, while the EOD
waveforms of neither of the androgen‑treated juveniles assumes the adult
male waveform (A) or the 12d transitional male wave- forms. Note: while the EODs of captive
males and females purportedly become more pronounced (Bass and Hopkins, 1984,
1985: Bass, 1986b), according to the authors, the female control shown did not change in
captivity. Also note that DHT appears to
have a more profound effect than
17‑MT. Modified after Hopkins and Bass (1981) and Bass and
314 Sex, hormones, environment and the captivity model
Brienomyrus sp. (syn. Brienomyrus sp. 2)
(both imported from
EODs from male and female Brienomyrus sp. maintained under laboratory conditions are almost
identical (Bass and Hopkins, 1984). The fish's EOD has
also been subjected to the influence of steroid hormones (Bass and Hopkins,
1984; Bass, 1986b). Bass and Hopkins (1984) reported that 17- MT, DHT, and CHOL, pellet implants lowered
the PPSFs in gonadectomized and intact mates and females, with the effects of
CHOL, being much smaller than those for both androgens. CHOL has also been
shown to have effects on electrocyte
characteristics in the male direction intermediate between controls and T‑treated
fish (Bass et al., 1986b). Thus, a close inspection of methods and results
sections and a comparison of Bass and
Hopkins (1984)
with Bass and Hopkins (1985) does not allow an unambiguous answer about the effects of CHOL, on the EOD
in Brienomyrus sp. For example, in one study (Bass and Hopkins, 1984), CHOL‑implanted
gona-dectomized females (n = 2) showed a 600 Hz drop in
PPSF compared with a 500 Hz drop in gonadectomized controls; while in another
study (Bass et al., 1986a), CHOL‑implanted
intact females (n = 3) exhibited a final average PPSF at least 500 or 600 Hz lower
than non‑treated females and males, respectively. A well‑designed
study with the proper controls should be performed before the conclusion that
"the effects of steroids on the EOD waveform are specific to gonadal
steroids" (Bass and Hopkins, 1985, p. 601) can be made. Although Bass and
Hopkins (1984) concluded that the EODs were also elongated by the steroid
treatments, EODs are presented for only two androgen‑treated fish and no
quantitative data are presented.
Brienomyrus brachyistius
(biphasic) (
B. brachyistius (biphasic) purportedly has no EOD‑related
sex difference (Hopkins, 1980, 1981a). 17‑MT added to the water of three
juvenile males and three adult females did not affect the EOD (Bass and
Hopkins, 1983). This is surprising since no other mormyrid species treated with
androgens has failed to show some hormone‑related
effects on the EOD.
Brienomyrus brachyistius
(imported from
Newly imported B. brachyistius exhibited a statistically significant sex dif-ference in the P2/P3 duration ratio of their EOD, with
males displaying lower ratios than females (Fig. 13.4 (A);
Landsman and Moller, 1991; in prep.). Androgens and CHOL, but not estrogen,
significantly influenced the durations of phases 2 and 3 of the EOD in
laboratory‑maintained fish not exhibiting the EOD‑related sex difference,
with androgen‑treated fish exhi-biting male‑like EODs ( Landsman
and Moller, 1993, in prep. ). Silastic
Sex‑related
and hormonally‑induced EOD plasticity 315
Fig. 13.4 (A) FODs of
male and female Brienomyrus brachyistius
(imported from
implants containing T and 11‑KT (11‑KT:
n = 1 male and 1 female; there was no difference in effects from T and 11‑KT),
17‑MT. and CHOL significantly increased the durations of both phases to
different degrees (Landsman and Moller, unpublished). However, by day 7, only
the two naturally occurring androgens, T and 11‑KT, resulted in a
significant decrease in the P2/P3 duration ratio compared with pre‑implant
ratios and with those of non‑handled or blank‑implanted controls.
Neither E2 nor CHOL exerted any significant effect on the sex‑related
duration ratio, while 17‑MT caused a gradual decrease in this ratio by
day 13 of treatment (Fig. 13.4 (B)).
316 Sex, hormones,
environment and the captivity model
Pollimyrus isidori
The triphasic EOD of P. isidori
exhibits a sex difference in the P1/P3
amplitude ratio (phases 1 and 3 are
positive, phase 2 is negative). Males exhibit a smaller P1 and a larger P3 amplitude, and females a larger P1 and
a smaller P3 amplitude (Fig. 13.5). This results in male ratios being
lower than female ratios (Westby and Kirschbaum, 1982; Bratton and Kramer,
1988; Crawford, 1992). When artificially induced breeding seasons were
introduced, females exhibited amplitude ratios that were threefold larger than
males (Crawford, 1992). Westby and Kirschbaum (1982) and Crawford (1992) found
almost no overlap between the sexes in this ratio, while others (Bratton and
Kramer, 1988) found a largely overlapping, but statistically significant, sex
difference.
While
some reported consistent lower PPSFs for males than females (Westby and
Kirschbaum, 1982), others found extensive overlap of PPSFs and no difference in
EOD duration between the sexes (Bratton and Kramer, 1988; Crawford, 1992).
Alteration of water conductivity conditions eliminated these sex differences
(section 13.3), leading some authors
to conclude that such differences did not function in species or sexual
identification (Bratton and Kramer, 1988). To date, no published studies have
investigated the potential of sensitivity to hormones in this species, so it is
impossible to predict natural sex differences based on hormonal milieu.
Hippopotamyrus batesii
According to Bass and Hopkins (1985), the EOD
waveform of one mature male H. batesii was twice as long
as that for
two mature females, when
Fig. 13.5 EOD waveform of a male and female Pollimyrus isidori (conductivity: 100 µS/cm). Subjects were selected to demonstrate a presumed sex difference in EOD. P1, first head‑positive phase; P2, head‑negative phase; P3, second head‑positive phase. Note that the ratio of P1 /P3 phase amplitudes is < 1.0 in this male, and > 1.0 in this female. Modified after Bratton and Kramer (1988).
Sex‑related
and hormonally‑induced EOD plasticity 317 317
data were recorded after an unspecified period
of time following capture in
Stomatorhinus corneti
Juvenile S.
corneti undergo a transitional stage
in the development of the adult EOD waveform (Bass and Hopkins, 1985). The
adult male EOD appeared to be longer in duration than that of the female (Fig.
13.6). When juveniles and one female were treated with 17‑MT, or T
propionate (two juveniles, one female), their EODs showed dramatic downshifts
in PPSF and increases in duration, both characteristic of male EODs (Bass and
Hopkins, 1985). However, no cholesterol or blank implants were used, and only
one untreated male served as a control.
Fig. 13.6 EOD waveforms of Stomatorhinus corneti. Juveniles
and females show two EOD forms depending on total body length (A, B, D). The
EOD of mature males typically has a reduced second positive peak (point 4) and
is longer in duration (C, three EODs superimposed). Testosterone propionate
added to the water of a female induces a mature male‑like EOD over a five
day period (D‑F). Modified after Bass and Hopkins (1985).
318 Sex, hormones, environment and the captivity model
Gnathonemus petersii
Fish obtained during the Nigerian rainy breeding
season and studied on the day they arrived exhibited EOD‑related sexual
dimorphisms: non‑overlapping sex differences in the durations of phases 2
and 3 (the major positive and negative phases) and in the PPSF of the EOD
(Landsman, 1993b). Males exhibited longer durations for both phases and lower
PPSFs than females (Fig. 13.7; Landsman, 1993b). No sex differences were
reflected in the duration of P1, P4, the total EOD or in the duration or
amplitude ratios of P2 to P3.
The
discovery of such a natural sex difference was surprising in light of two
earlier incongruent reports by Kramer and Westby (1985), who did not find a
waveform‑related sex difference (section 13.3), and Landsman et al. (1987), who reported that males
displayed higher PPSFs (and thus shorter EODs!) than females, provided the fish
were unrestrained (section 13.3). These incongruent findings were resolved and
will be discussed in section 13.4. The natural sex differences in the EOD in G. petersii
are consistent with the results of exogenous hormone treatment in this
species (Landsman and Moller, 1988; Landsman et al., 1990).
Androgens
affect the durations of P2 and P3 of the EOD in juvenile and adult G. petersii,
and consequently affect the PPSFs (Fig. 13.8). Landsman and Moller (1988)
and Landsman et al. (1990) demonstrated
that both low and high doses of 17‑MT, T and DHT (administered through
silastic implants) significantly increase the durations of P2 and P3 in both
gonadectomized juveniles (Figs 13.8, 13.9A) and gonadectomized adult males and
females (Fig. 13.9B), while E2 and CHOL have no effect on these
phases (Figs 13.8, 13.9A, low‑ and high‑dose). The androgens 17‑MT
and T decreased the PPSFs in both juveniles (Fig. 13.9A) and adults (Fig.
13.9B), while DHT had no effect on PPSF at low dose and was less potent than T
at the high dose (Fig. 13.9A).
Surprisingly,
E2 caused a slight, but significant, increase in PPSFs in adults
(Fig. 13.9B), but not in juveniles (Fig. 13.9A). This is interesting for a
number of reasons, since it is the only reported E2 effect on the
EOD in mormyrid fish that worked in the direction opposite to that of
androgens. Plasma E2 levels in adults implanted with E2
were about fourfold higher than in juveniles when both were administered the
same dose of this hormone (Landsman et
al., 1990) (Fig. 13.10). This difference in plasma E2 levels in G. petersii
implanted with E2 may have been a function of age-related
differences in hormone metabolism rates (Harding, 1986). Thus, the effects on
the adult EOD not present in juvenile EODs may have been a function of hormone
levels and/or stage of receptor development.
A male‑like
EOD was induced in immature and adult B.
brachyistius (triphasic)
by treatment with E2
( Bass and Hopkins,
1985 )
and, as
Sex‑related and hormonally‑induced
EOD plasticity 319 319
