8 B
. Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
trials using the ratios of 19:1, 15:5, 10:10, 5:15, 1:19 and 0:20. The Tukey–Kramer test for multiple comparisons of mean percentages was performed because a significant
difference was indicated by the ANOVA test Sokal and Rohlf, 1995. Mean arrival and mean feeding times were calculated for each species at each ratio
and were plotted on graphs showing their variation with the changing ratio of the numbers of Nassarius festivus to Diogenes edwardsii. A Kruskal–Wallis test was
performed to compare the arrival times among the different ratios for each species. A nonparametric test was used because of the non-normal distribution of the data Sokal
and Rohlf, 1995. Feeding times were also analyzed in the same way. Tests that indicated significant differences were further analyzed by a Mann–Whitney U-test for
pairwise comparisons Sokal and Rohlf, 1995. The computer software JMP was used for all statistical analyses except the Mann–Whitney U-test Sall and Lehman, 1996.
3. Results
3.1. Food preferences All the four baits, i.e. fish, bivalve, soldier crab and shrimp, attracted far greater
numbers of Nassarius festivus than Diogenes edwardsii and Clibanarius infraspinatus Table 4. The attractiveness of the four different baits to each of the three species was
analyzed by a chi-square test for goodness of fit. When the data from the six experiments for each of the species were pooled, the chi-square test showed that, for all three, the
numbers of individuals attracted to the four baits were significantly different N
. festivus:
2 2
x 5 317.43, df 5 3, P , 0.001; D. edwardsii: x 5 36.37, df 5 3, P , 0.001; C.
2
infraspinatus: x 5 25.20, df 5 3, P , 0.001. Fish and bivalve baits attracted greater
numbers of all three species. The chi-square test for goodness of fit comparing the numbers of N
. festivus attracted to their two favourite food items, i.e. fish and bivalve, suggested that the latter was preferred by a significantly higher number of N
. festivus
2
than the former x 5 53.66, df 5 1, P , 0.001. Conversely, the same statistical tests
demonstrated that the numbers of hermit crabs attracted to their two favourite baits, fish
Table 4 Cumulative numbers six experiments of Nassarius festivus, Diogenes edwardsii and Clibanarius infras-
pinatus attracted to four different baits at Starfish Bay in October 1998. The attractiveness of the four different
a
baits to each of the three species was analyzed by a chi-square test for goodness of fit
2
Species Bait
df x
P Fish
Bivalve Soldier crab
Shrimp Nassarius festivus
1333 1739
1114 878
3 317.43
, 0.001 222.2
289.8 185.7
146.3 Diogenes edwardsii
25 30
2 6
3 36.37
, 0.001 4.2
5.0 0.3
1.0 Clibanarius infraspinatus
20 21
1 6
3 25.20
, 0.001 3.3
3.5 0.2
1.0
a
The mean numbers of each species per bait are given in parentheses.
B . Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
9
and bivalve, were insignificantly different for both D . edwardsii and C. infraspinatus D.
2 2
edwardsii: x 5 0.45, df 5 1, P . 0.05; C. infraspinatus: x 5 0.02, df 5 1, P . 0.05.
3.2. Sequence of arrival and departure The results of the seven feeding experiments conducted in the field are illustrated in
3
Fig. 1. After 5 min, fish baits of 1 cm each had attracted a mean of five Nassarius festivus. The mean number of Clibanarius infraspinatus arriving at the bait was,
however, less than 1. No Diogenes edwardsii arrived within 5 min. The numbers of N .
festivus attracted to the bait increased rapidly up to a mean of about 28 after 15 min and peaked at a mean of 41 after 30 min. Thereafter, an increasing number of N
. festivus departed the bait. The bait was consumed after | 60 to 70 min. All individuals had
departed after 75 min. Conversely, the numbers of D . edwardsii and C. infraspinatus
Fig. 1. Results of seven scavenger feeding experiments showing the mean numbers of A Nassarius festivus and B Diogenes edwardsii and Clibanarius infraspinatus attracted to fish bait at Starfish Bay in October
1998. Bars indicate standard error of the mean.
10 B
. Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
attracted to the bait remained low, and were far less than N . festivus throughout the
experiment. The mean numbers of the two species of hermit crabs did not exceed three. Both showed a similar pattern of arrival and departure at the bait. Numbers for both
species increased slowly until they peaked at 55 min, with a mean of 2.3 and 1.7 for D .
edwardsii and C . infraspinatus, respectively. Individual numbers reached a maximum,
25 min later than N . festivus. The times at which all individuals departed the bait were
70 and 75 min for C . infraspinatus and D. edwardsii, respectively.
It should be noted that, although both species of hermit crabs were attracted to the bait, some which arrived late were unable to find their way through the large
congregation of Nassarius festivus surrounding the fish so as to feed. They either grasped some of the feeding N
. festivus or remained stationary nearby. Those which arrived early, however, and managed to climb over the N
. festivus did eat. 3.3. Food detection distance
Nassarius festivus was able to locate the fish carrion from all distances up to 80 cm Table 5. When the data from the five experiments were pooled, over 50 of the total
number of N . festivus from each of the tested distances reached the food. They were
considered to be within the detection distance of the bait by application of the 50 rule. The chi-square test for goodness of fit showed no significant difference in the numbers
2
of N . festivus arriving at the bait from any of the tested distances x 5 2.0, df 5 7,
P . 0.05. Although it can be suggested that such an insignificant difference was due to random encounters of N
. festivus with the bait, it is more likely that 80 cm is less than the maximum food detection distance of | 2.5 m Britton and Morton, 1992. This is
reflected by the significant difference in the arrival times to food by individuals from different distances according to one-way ANOVA using the pooled data from the five
experiments F 5 4.90, P , 0.0001. There was a trend of increasing arrival time at fish carrion with distance Fig. 2A.
Conversely, the percentages of the total number of Diogenes edwardsii reaching the carrion from all the tested distances were less than Nassarius festivus Table 5. Since
all percentages were , 50, none of the tested distances was considered to be within the detection range of D
. edwardsii. When the data from the five experiments were
Table 5 Cumulative numbers five experiments of Nassarius festivus and Diogenes edwardsii arriving at fish carrion
21
from various distances in seawater flowing at 3 mm s . The numbers of arrivals from different distances were
a
analyzed by a chi-square test for goodness of fit for each species
2
Species Distance from carrion cm
df x
P 10
20 30
40 50
60 70
80 Nassarius festivus
20 20
19 18
17 18
17 13
7 2.0 . 0.05
100 100
95 90
85 90
85 65
Diogenes edwardsii 7
4 7
3 2
4 3
2 7
7.0 . 0.05 35
20 35
15 10
20 15
10
a
The percentages of the total numbers of individuals reaching the carrion are given in parentheses.
B . Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
11
Fig. 2. The mean arrival times at fish carrion by A Nassarius festivus and B Diogenes edwardsii positioned
21
at various distances from it in seawater flowing at 3 mm s . Numerals indicate the numbers of individuals
represented by each data point. Bars indicate the standard error of the mean.
pooled, a chi-square test for goodness of fit demonstrated that there was no significant
2
difference in the numbers of D . edwardsii arriving from different distances x 5 7.0,
df 5 7, P . 0.05. No significant difference in arrival times from different distances was detected by one-way ANOVA using the pooled data F 5 1.71, P 5 0.1524. No clear
relationship between arrival time and distance was, therefore, revealed Fig. 2B. These data suggest that the food detection distance of D
. edwardsii was , 10 cm and it appeared to move randomly in the tank until it was in close proximity to the food and
reached its food detection distance. It then moved towards it. When the mean arrival times at food by the two species were compared, Nassarius
festivus arrived from all distances except 80 cm and, on average, earlier than Diogenes edwardsii Fig. 2. The arrival times by D
. edwardsii from each of the tested distances showed greater variation than N
. festivus. The former standard errors were all . 2 min, except for the one corresponding to a distance of 80 cm, whereas the latter standard
errors were all , 2 min.
12 B
. Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
3.4. Time spent feeding and consumption Correlation coefficients for the data related to wet and dry body weights log against
e
shell length of Nassarius festivus and Diogenes edwardsii were highly significant N .
festivus: r 5 0.9416 and 0.9376, respectively; D . edwardsii: r 5 0.9761 and 0.9760,
respectively where P , 0.0001. The regression equations obtained were used to estimate the initial wet and dry body weights of the animals before they fed upon the
fish carrion. Similarly, the correlation coefficient for the data related to dry tissue weight against wet tissue weight of fish carrion was highly significant r 5 0.9975, P , 0.0001.
The regression equation obtained was used to estimate the dry weights of fish carrion prior to feeding by Nassarius festivus and Diogenes edwardsii.
The results of the five consumption experiments on Nassarius festivus and Diogenes edwardsii are summarized in Table 6. Data from the five experiments were pooled. The
percentage of the total numbers of N . festivus feeding on the carrion was very high
96 and was greater than D . edwardsii 69. The mean time spent feeding on a
single meal by N . festivus was 13.20 min Table 6. The equivalent figure for D.
edwardsii could not, however, be estimated as some individuals continued to eat at the end of the experimental time. The time spent feeding by D
. edwardsii thus varied considerably from 0.28 min to 119.75 min during the 2-h experiments Table 6.
The mean consumption rates for Nassarius festivus were calculated to be 0.124 mg
21 21
wet weight and 0.034 mg dry weight of food individual min
. The equivalent figures for Diogenes edwardsii were 0.003 mg and 0.001 mg, respectively Table 6. When
these figures were compared between the two species, the amount of food eaten
21 21
individual min
by N . festivus was over 30 times that of D. edwardsii.
Table 6 Summary of the results of the five consumption experiments using Nassarius festivus and Diogenes edwardsii
a
feeding on fish carrion Nassarius festivus
Diogenes edwardsii Total number feeding
96 69
Percentage of animals feeding 96
69 Mean time spent feeding on a
13.2064.73 –
single meal min 5.45, 28.50
0.28, . 119.75 Mean time spent feeding during
13.20 60.72
the experiment min Mean consumption rate
21 21
mg wet weight ind min
0.123560.0432 0.003460.0014
0.0642, 0.1850 0.0012, 0.0045
21 21
mg dry weight ind min
0.033660.0126 0.001060.0004
0.0166, 0.0486 0.0007, 0.0015
21
Mean wet body weight min 1.4
0.1 with shell removed
21
Mean dry body weight min 1.3
0.1 with shell removed
a
Mean6S.D.; values in parentheses represent the range. The mean time spent feeding on a single meal by D
. edwardsii could not be estimated as some individuals continued to eat the bait at the end of the experimental time.
B . Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
13
When the consumption rates were expressed in terms of the percentage wet and dry
21
body weights consumed min , Nassarius festivus consumed a mean of 1.4 of its own
21 21
wet body weight min 18.5 average feeding bout
and a mean of 1.3 of its own
21 21
dry body weight min 17.2 average feeding bout
. Conversely, Diogenes
21
edwardsii only consumed a mean of 0.1 of its own wet and dry body weights min Table 6. N
. festivus thus ate 13 to 14 times faster than D. edwardsii. The mean consumption rates, which were expressed in terms of percentage body weight consumed
21
min , were calculated based on a reduced data set. This was because a few percentage
values were negative, and eliminated from the analysis. As a result, the size of the final data set was reduced to 88 N
. festivus individuals and 61 D. edwardsii individuals. 3.5. Behaviour when feeding together
A clear sequence of behaviour associated with feeding by Nassarius festivus was shown. Figs. 3, 4A, 5A, 6A, 7A and 8A correspond to the ratios of the numbers of N
. festivus to Diogenes edwardsii, i.e. 20:0, 19:1, 15:5, 10:10, 5:15 and 1:19, respectively.
The patterns of behaviour were similar for all these ratios. They first moved randomly in the tray, followed by directed movement towards the carrion and commenced feeding.
At 5 min, . 60 of N . festivus had fed upon the food in all cases Figs. 3–8. The
Fig. 3. Behaviour of 20 Nassarius festivus when they were allowed to feed together in the absence of Diogenes edwardsii. The percentage of the total number of individuals showing a certain behaviour was
calculated using the pooled data from three experiments, i.e. a total of 60 N . festivus were used.
14 B
. Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
Fig. 4. Behaviour of A Nassarius festivus and B Diogenes edwardsii when they were allowed to feed together in the ratio of 19:1. The percentage of the total number of individuals showing a certain behaviour
was calculated using the pooled data from three experiments, i.e. a total of 57 N . festivus and three D.
edwardsii were used interspecific interaction — cheliped contact of moving-out N . festivus by D. edwardsii.
B . Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
15
Fig. 5. Behaviour of A Nassarius festivus and B Diogenes edwardsii when they were allowed to feed together in the ratio of 15:5. The percentage of the total number of individuals showing a certain behaviour
was calculated using the pooled data from three experiments, i.e. a total of 45 N . festivus and 15 D. edwardsii
were used interspecific interaction — cheliped contact of moving-out N . festivus by D. edwardsii;
interspecific interaction — grasping of feeding moving-out N . festivus by D. edwardsii; interspecific
interaction — manipulation of feeding N . festivus by D. edwardsii; intraspecific interaction among D.
[ [[
edwardsii — manipulation; intraspecific interaction among D
. edwardsii — cheliped strike.
16 B
. Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
Fig. 6. Behaviour of A Nassarius festivus and B Diogenes edwardsii when they were allowed to feed together in the ratio of 10:10. The percentage of the total number of individuals showing a certain behaviour
was calculated using the pooled data from three experiments, i.e. a total of 30 N . festivus and 30 D. edwardsii
were used interspecific interaction — grasping of feeding moving-out N . festivus by D. edwardsii;
interspecific interaction — manipulation of feeding N . festivus by D. edwardsii; intraspecific interaction
[ [[
among D . edwardsii
— manipulation; intraspecific interaction among D . edwardsii
— cheliped strike.
B . Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
17
Fig. 7. Behaviour of A Nassarius festivus and B Diogenes edwardsii when they were allowed to feed together in the ratio of 5:15. The percentage of the total number of individuals showing a certain behaviour
was calculated using the pooled data from three experiments, i.e. a total of 15 N . festivus and 45 D. edwardsii
were used interspecific interaction — cheliped contact of feeding moving-out N . festivus by D. edwardsii;
interspecific interaction — grasping of feeding N . festivus by D. edwardsii; interspecific interaction —
manipulation of feeding moving-out N . festivus by D. edwardsii; intraspecific interaction among D.
[ [[
edwardsii — manipulation; intraspecific interaction among D
. edwardsii — cheliped strike; intraspecific
[[[
interaction among D . edwardsii
— ambulatory display.
18 B
. Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
Fig. 8. Behaviour of A Nassarius festivus and B Diogenes edwardsii when they were allowed to feed together in the ratio of 1:19. The percentage of the total number of individuals showing a certain behaviour
was calculated using the pooled data from three experiments, i.e. a total of three N . festivus and 57 D.
edwardsii were used interspecific interaction — manipulation of feeding N . festivus by D. edwardsii;
[ [[
intraspecific interaction among D . edwardsii
— manipulation; intraspecific interaction among D . edwardsii
[[[
— cheliped strike; intraspecific interaction among D . edwardsii
— ambulatory display.
B . Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
19
percentage could be as high as 100, as in the experiment using the ratio of 1:19 Fig. 8. For all the six ratios, the percentage of N
. festivus feeding peaked at a value of about or . 90 at 5 to 10 min. Feeding was observed to be the dominant behaviour between 5
to 15 min. After feeding, they moved away from the food. Subsequently, they either moved around in the tray or remained stationary. The latter behaviour was observed to
be the most common . 46 at 25 to 30 min.
Unlike Nassarius festivus, the sequence of behaviour associated with feeding by Diogenes edwardsii is less clearly shown in Figs. 4B, 5B, 6B, 7B, 8B and 9, which
correspond to the ratios of 19:1, 15:5, 10:10, 5:15, 1:19 and 0:20, respectively. It was, however, similar to that of N
. festivus, i.e. moving randomly, moving towards, feeding, moving away and either moving or remaining stationary away from food, except that D
. edwardsii often stopped feeding and grasped the food with their chelipeds for some time
before resuming. Some also remained stationary near the food before approaching it; such behaviour was recorded during the 5 to 20 min period in Fig. 5B. Some approached
and ate more than once. Some D . edwardsii, usually those some distance from the food,
Fig. 9. Behaviour of 20 Diogenes edwardsii when they were allowed to feed together in the absence of Nassarius festivus. The percentage of the total number of individuals showing a certain behaviour was
calculated using the pooled data from three experiments, i.e. a total of 60 D . edwardsii were used intraspecific
[ [[
[[[
interaction — manipulation; intraspecific interaction
— cheliped strike; intraspecific interaction —
ambulatory display.
20 B
. Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
either moved or remained stationary showing no other behaviours. That is, not all individuals fed during the experiments.
The patterns of behaviour of Diogenes edwardsii were not similar in the experiments using different ratios. The remaining stationary behaviour away from the food was
common when the ratios of 19:1 and 15:5 were used Figs. 4B and 5B. For the ratios of 10:10, 5:15, 1:19 and 0:20, the behaviour shown by a majority of D
. edwardsii 35–70 was moving randomly in the tray Figs. 6 to 9. The percentage of D
. edwardsii feeding varied with changes in the ratio. None of the individuals fed at the
ratio of 19:1 Fig. 4B. At the ratio of 15:5, D . edwardsii began to feed after 10 min
Fig. 5B. As the number of Nassarius festivus declined and the numbers of D .
edwardsii increased, an increasing percentage of the hermit crab either fed or grasped the food at an earlier time. At the ratio of 0:20, . 13 of them either fed or grasped the
food throughout the 30-min experiment Fig. 9. Unlike N . festivus, for which the
percentage of feeding individuals always peaked in the early stages of the experiment, the percentage of D
. edwardsii which either fed or grasped the food increased slowly. Intra- and interspecific interactions were also investigated. No intraspecific interaction
among Nassarius festivus individuals was detected. Conversely, intraspecific interactions among Diogenes edwardsii, including manipulation, cheliped strike and ambulatory
display, were observed Figs. 5–9. The intraspecific interactions increased when numbers increased and the numbers of N
. festivus decreased, but remained at 12 after the ratio of 1:19 was reached Fig. 10A.
Interspecific interactions between Nassarius festivus and Diogenes edwardsii were detected. Such interactions involved cheliped contact, grasping and manipulation of the
former by the latter Figs. 4–8. Numbers of interspecific interactions were greater at the ratios of 15:5, 10:10 and 5:15 Fig. 10B, i.e. they fell when the numbers of N
. festivus increased and those of D
. edwardsii decreased, and vice versa. 3.6. Percentage feeding, arrival time and time spent feeding when together
All nassariids fed upon the carrion in all the experimental trials at ratios of Nassarius festivus to Diogenes edwardsii of 20:0, 19:1, 15:5, 10:10, 5:15 and 1:19 Fig. 11. Even
though the numbers of D . edwardsii increased from 0 to 19, all N. festivus were able to
feed. Conversely, the percentages of the total number of D . edwardsii feeding upon the
carrion were never . 65 Fig. 11. One-way ANOVA showed a significant difference in the percentages of the total number of D
. edwardsii feeding among the experiments using the ratios of 19:1, 15:5, 10:10, 5:15, 1:19 and 0:20 F 5 24.29, P , 0.0001. The
Tukey–Kramer test for multiple comparisons showed that the mean percentages of the total numbers of D
. edwardsii feeding at the ratio of 19:1 was significantly lower than that for the other five ratios and that the ratio of 15:5 was also significantly lower than
that of the other ratios, except 19:1 P , 0.05. This means that the percentage number of D
. edwardsii feeding increased with a decreasing number of N. festivus and an increasing number of D
. edwardsii, but such a percentage levelled off when the numbers of the former fell to 10 and the latter rose to 10 Fig. 11.
The Kruskal–Wallis test detected no significant difference in the arrival times of Nassarius festivus among the trials of different ratios H 5 2.64, df 5 5, P 5 0.7551.
B . Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
21
Fig. 10. The total numbers of A intraspecific interactions among D . edwardsii and B interspecific
interactions between N . festivus and D. edwardsii recorded during the 30-min experiment, using the pooled
data from three trials, when different ratios of the number of N . festivus to D. edwardsii were used. The
numbers of these two kinds of interactions were recorded at 5-min intervals.
Similarly, the arrival times of Diogenes edwardsii differed insignificantly H 5 3.27, df 5 4, P 5 0.5133, i.e. there was no obvious trend in the mean arrival time with
changes in the ratio of the number of N . festivus to D. edwardsii for each species Fig.
12. The feeding times of both Nassarius festivus and Diogenes edwardsii were shown to
differ significantly among the trials using different ratios, as analyzed by the Kruskal– Wallis tests N
. festivus: H 5 44.19, df 5 5, P , 0.0001; D. edwardsii: H 5 9.60, df 5 4, P 5 0.0477. The feeding times of N
. festivus at the ratios of 20:0 and 19:1 were
22 B
. Morton, W.Y. Yuen J. Exp. Mar. Biol. Ecol. 246 2000 1 –29
Fig. 11. The percentages of the total numbers of Nassarius festivus and Diogenes edwardsii feeding upon fish carrion when they were allowed to feed together in different ratios.
significantly lower than those at the ratios of 15:5 and 10:10 Mann–Whitney U-test for pairwise comparisons: z 5 4.30 for 20:0 vs. 15:5; z 5 5.35 for 20:0 vs. 10:10; z 5 3.15
for 19:1 vs. 15:5; z 5 4.66 for 19:1 vs. 10:10; P , 0.0001 for all the above four pairs. The Mann–Whitney U-test for pairwise comparisons showed that N
. festivus, at the ratio of 5:15, fed for a significantly shorter time than those at a ratio of 10:10, but
significantly longer than those at a ratio of 20:0 z 5 2 2.84, P 5 0.0023 and z 5 2.55, P 5 0.0054, respectively. These observations indicate that the mean feeding time of N
. festivus increased when its number fell from 20 to 10 and the numbers of D
. edwardsii increased from 0 to 10, but decreased slightly when numbers dropped further to 1 and
the numbers of the hermit crab increased further to 19 Fig. 13A. The Mann–Whitney U-test for pairwise comparisons suggested that the feeding times
of Diogenes edwardsii at the ratios of 15:5 and 10:10 were both significantly shorter than those at the ratio of 0:20 z 5 2 2.20, P 5 0.0139 and z 5 2 2.75, P 5 0.0030,
respectively. These data imply that the mean feeding time of D . edwardsii increased
with an increasing number of conspecifics and a decreasing number of Nassarius festivus Fig. 13B.
4. Discussion
