Conceived and designed the experiments: LCD DRB. Performed the experiments: LCD. Analyzed the data: LCD CHG JKT. Contributed reagents/materials/analysis tools: LCD CHG JKT DRB. Wrote the paper: LCD CHG JKT DRB.
The authors have declared that no competing interests exist.
Diver-based Underwater Visual Censuses (UVCs), particularly transect-based surveys, are key tools in the study of coral reef fish ecology. These techniques, however, have inherent problems that make it difficult to collect accurate numerical data. One of these problems is the diver effect (defined as the reaction of fish to a diver). Although widely recognised, its effects have yet to be quantified and the extent of taxonomic variation remains to be determined. We therefore examined relative diver effects on a reef fish assemblage on the Great Barrier Reef. Using common UVC methods, the recorded abundance of seven reef fish groups were significantly affected by the ongoing presence of SCUBA divers. Overall, the diver effect resulted in a 52% decrease in the mean number of individuals recorded, with declines of up to 70% in individual families. Although the diver effect appears to be a significant problem, UVCs remain a useful approach for quantifying spatial and temporal variation in relative fish abundances, especially if using methods that minimise the exposure of fishes to divers. Fixed distance transects using tapes or lines deployed by a second diver (or GPS-calibrated timed swims) would appear to maximise fish counts and minimise diver effects.
SCUBA diving has greatly facilitated the collection and sampling of fishes on coral
reefs. Underwater Visual Censuses (UVCs) are the most popular and practical method
for studying the distribution and abundance of tropical reef fish populations
One potentially serious but poorly understood problem in UVC sampling is the reaction
of the fish to the diver: the diver effect
Despite all their problems, UVCs remain by far the most popular method available for
surveying reef fish populations
The interaction between sampling method and a species' behaviour was recognised
over 30 years ago
Clearly, it is important to determine the magnitude of different sources of variation
in abundance data and the sensitivity of measures to inherent biases in the
methodology
All activities are covered and approved by James Cook University Animal Ethics Review Committee (approval identification A1412). Only visual censuses of fish were conducted during this study; no animals were collected or manipulated.
All observations were undertaken during April and May 2009 at three sites along
the reef crest of Pioneer Bay, located on the leeward side of Orpheus Island
(18°35′S, 146°20′E), an inner-shelf island on the Great
Barrier Reef (GBR), Australia. Orpheus Island, one of the Palm Islands, is a
granitic continental island in the central section of the Great Barrier Reef
Marine Park. Pioneer Bay has a well-developed fringing reef, typical of
inner-shelf GBR reefs, with an extensive reef flat stretching approximately 150
m from the shoreline out to the reef crest (depth of 2–4 m) and down the
reef slope to approximately 20 m
Our goal was to quantify the relative magnitude of the diver effect in three
different census methods. Prior to censuses, locations along the reef crest with
similar benthic configurations were identified within the three sites and marked
with buoys. All censuses were conducted within three hours of high tide between
1000 and 1500 hrs to minimise confounding tide or time-of-day effects. To avoid
localised disturbance the dive team entered the water at least 20 m from the
site marker buoy, descended to the appropriate depth (2–3 m deep, 1 m
above the substratum) and prepared for the survey (following
As the majority of papers use tape transects (but with limited detail of how they
were performed) we identified the three extreme cases in order to maximise
differences in potential diver effects. The first was a 50 m fixed distance
transect (while laying a 50 m fibreglass tape). Fishes were counted by an
observer followed closely by a second diver laying the tape and stopping the
observer after 50 m. This method was initially developed to minimise diver
disturbance prior to counting
Immediately after the fixed distance transect, fishes were re-censused along the 50 m tape to simulate the traditional practice of counting fishes after having laid a 50 m tape (the second diver following the observer to maintain the buddy pair). In this transect, fishes are exposed to the initial disturbance and the presence of the tape. Although recognised as a ‘diver effect’ it represents a complex response to ongoing diver presence and a ‘tape effect’ due to the presence of the tape. These two effects are invariably associated using this standard methodology.
Finally, fishes were counted again along the existing tape following a 5 minute
acclimation period (as per
In our analyses we compared the number of fishes recorded on each transect, i.e. the number of individuals per 250 m2. This metric was selected as it is the primary metric used in reef fish studies undertaking tape transects (in the literature survey over 90% of studies were recording fish densities, i.e. numbers per unit area). It is also the most likely to be responsive to diver effects (rather than species richness). In the analyses, we first compared the fixed distance and immediate censuses. As they were covering the same area, the samples were non-independent and densities were therefore examined using paired t-tests on total fish densities and densities within each of the focal taxa. To investigate the extent to which a 5 minute acclimation period would reduce the diver effect, the initial count was also compared to the final count (after the tape had been swum over twice). Prior to analyses, all data were log transformed (log10 n +1) to ensure that homogeneity of variance and normality were within acceptable limits. In all t-tests, a Bonferroni correction was used, resulting in an adjusted alpha-level (i.e. α = 0.05/8 = 0.006).To examine the variation in the abundance of individual species in the three separate censuses (fixed distance, immediate and after 5-minutes), mean species' abundances were examined using a principal component analysis (PCA; covariance analysis of log10 n +1 transformed data).
In terms of all taxa combined, the immediate return tape transect yielded less than
half the number of fishes recorded using the initial fixed distance transect, with
only 12.8±0.8 (mean ± SE) fishes compared to 26.5±1.7,
respectively (
Relative diver effects on estimated reef fish densities comparing counts over
a fixed distance 50 m transect and counts along the tape immediately after
deployment. Values indicate the proportional decrease in abundance;
asterisks represent significant differences using a Bonferroni corrected
alpha-value (
|
|
|
|
Overall fish abundance | 12.495 | 59 |
|
Acanthuridae | 3.948 | 59 |
|
Chaetodontidae | 2.964 | 59 |
|
Labridae | 3.540 | 59 |
|
Lutjanidae | 3.178 | 59 |
|
parrotfishes | 9.179 | 59 |
|
Serranidae | 2.041 | 59 | 0.046 |
Siganidae | 5.766 | 59 |
|
Paired t-tests showing differences for overall fish abundance and abundances within each family between fixed distance and immediate return tape transects. P-values marked in bold show significance (using Bonferroni adjusted alpha levels α<0.006).
Despite the rather large declines reported for the immediate transects, numbers did
recover to some extent after a 5 minute waiting period. Comparing the initial fixed
distance counts with those after the 5 minute waiting period resulted in a
difference in all fishes combined of just 27% (
Relative diver effects on estimated reef fish densities comparing counts over
a fixed distance 50 m transect and counts after a 5 minute waiting period.
Values indicate the proportional decrease in abundance, asterisks represent
significant differences using a Bonferroni corrected alpha-value
(
|
|
|
|
Overall fish abundance | 5.110 | 59 |
|
Acanthuridae | 3.666 | 59 |
|
Chaetodontidae | 0.717 | 59 | 0.476 |
Labridae | 0.707 | 59 | 0.482 |
Lutjanidae | 0.721 | 59 | 0.474 |
parrotfishes | 5.548 | 59 |
|
Serranidae | 0.036 | 59 | 0.971 |
Siganidae | 3.255 | 59 |
|
Paired t-tests showing differences for overall fish abundance and within each family between fixed distance and tape (after 5 minutes) transects. P-values marked in bold show significance (using Bonferroni adjusted alpha levels α<0.006).
The PCA (
(
We recorded a marked decline in fish abundance as a result of ongoing diver presence. Overall, there was a 52% decrease in the mean number of fish recorded between fixed distance and immediate tape transects. The maximum recorded decrease was 70% for parrotfishes. A comparable diver effect was found, to varying extents, in all reef fish groups examined.
The tendency of fish to avoid divers is supported by the literature in terms of both
the magnitude and nature of the diver effect
The findings of the present study, however, contrast with those of Watson and Harvey
The physiological basis for the negative reaction is not known. Of all stimuli, sound
is most frequently identified in diver avoidance
Our results suggest that vision is the main stimulus for the fishes encountered on
the transects. It appears that the ongoing visible presence of divers exerts a
negative diver effect and is largely responsible for the strong patterns seen in the
present study. This may be expected given the importance of the visual system for
coral reef fishes
Although the response to the diver appears to be the primary stimulus it must be
noted that there is also a possible ‘tape effect’. These two issues are
inextricably associated in the standard methodology, as fishes are exposed to the
ongoing presence of both the diver and tape. Although the tape effect appears to be
relatively small, some fishes have been observed to respond negatively to the tapes,
approaching them and then changing swimming direction or fleeing. A comparable
pattern was seen with stationary video quadrats which are now removed before filming
One additional limitation of the present study is that only those species that remain
visible can be recorded and considered in terms of diver-based reactions
The relative diver effect was evident to different extents among the seven groups
examined. This was statistically significant in six of the seven groups with mean
decreases of 29–70% from initial abundances. The herbivorous
parrotfishes, Acanthuridae and Siganidae
The Chaetodontidae and wrasses were two of the least-affected groups. Chaetodontids
are often closely associated with the structure of the benthic reef habitat
The diver-negative reactions recorded in the present study suggest that absolute
numbers, and therefore the functional impact of mobile reef fishes, may be
underestimated when using standard UVC techniques. In all 7 families, the immediate
return census was lower than the fixed distance count despite the fact that Pioneer
Bay has been exposed to active SCUBA-based research for more than 30 years
In the present study, the parrotfishes (a non-harvested species in a marine protected
no-take area) exhibited a 70% decrease in mean abundance (comparing the fixed
distance transect with the immediate return tape transect). Such variation calls for
caution when comparing studies using different methods. The magnitude of change and
the potential for further fishing-mediated variation in absolute and relative
densities are also of concern. The magnitude of the diver effect recorded herein
approximates the differences described in previous studies of parrotfish densities
in the literature related to MPAs (e.g.,
Our results suggest that the censusing of fishes after laying a measuring tape can
have a profound effect on fish counts. While this may not be detrimental for
analyses of relative abundances within a single study, it may severely limit our
ability to combine visual census data in meta-analyses, or to compare values among
studies. It appears that the most robust and accurate visual censuses will be based
on active recording, as in fixed distance transects (where the observer or a second
diver deploys a line
Recent publications have identified significant problems with tape-based transects.
This includes detectability, where small or cryptic fishes are only effectively
recorded close to the observer, and transect length effects, where there is an
anomalous peak in counts at the start and end of transects
Fortunately, as most studies are interested in spatial or temporal changes in the relative abundance of fishes (rather than absolute numbers), diver effects, if constant, will have only a limited effect on interpretations using existing data. Thus, while the diver effect cannot be completely eliminated from UVCs, awareness of its potential direction and magnitude will hopefully permit a better understanding of the abilities and limitations of UVCs.
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Sources used in literature evaluation.
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We thank P. Dickens, G. Dickens and Orpheus Island Research Station staff for field support and assistance and R. Alford, S. Connolly, R. Fox, A. Hoey, G. Jones, P. Munday, R. Rowe and three anonymous reviewers for helpful comments and suggestions.