First field studies of an Endangered South African seahorse, Hippocampus capensis

Environmental Biology of Fishes 67: 35–46, 2003.
© 2003 Kluwer Academic Publishers. Printed in the Netherlands.
First field studies of an Endangered South African seahorse,
Hippocampus capensis
Elanor M. Bella,∗ , Jacqueline F. Lockyearb , Jana M. McPhersona,∗∗ ,
A. Dale Marsdena,∗∗∗ & Amanda C.J. Vincenta,∗∗∗
a
Project Seahorse, Department of Biology, McGill University, 1205 Avenue Docteur Penfield,
Montréal, Québec, Canada H3A 1B1
b
Department of Ichthyology & Fisheries Science, Rhodes University, Grahamstown, South Africa
∗
Current address: Department of Ecology and Ecosystem Modelling, Institute of Biochemistry and
Biology, Potsdam University, Maulbeerallee 2, 14469 Potsdam, Germany (e-mail: ebell@rz.uni-potsdam.de)
∗∗
Current address: Department of Zoology, University of Oxford, South Parks Road,
Oxford OX1 3PS, UK
∗∗∗
Current address: Project Seahorse, Fisheries Centre, The University of British Columbia,
2204 Main Mall, Vancouver, B.C., Canada V6T 1Z4
Received 12 December 2001
Accepted 16 January 2003
Key words: Knysna Estuary, abundance, distribution, population structure, behaviour
Synopsis
South Africa’s endemic Knysna seahorse, Hippocampus capensis Boulenger 1900, is a rare example of a marine
fish listed as Endangered by the IUCN because of its limited range and habitat vulnerability. It is restricted to four
estuaries on the southern coast of South Africa. This study reports on its biology in the Knysna and Swartvlei
estuaries, both of which are experiencing heavy coastal development. We found that H. capensis was distributed
heterogeneously throughout the Knysna Estuary, with a mean density of 0.0089 m−2 and an estimated total population of 89 000 seahorses (95% confidence interval: 30 000–148 000). H. capensis was found most frequently in
low density vegetation stands (≤20% cover) and grasping Zostera capensis. Seahorse density was not otherwise
correlated with habitat type or depth. The size of the area in which any particular seahorse was resighted did not
differ between males and females. Adult sex ratios were skewed in most transects, with more males than females,
but were even on a 10 by 10 m focal study grid. Only three juveniles were sighted during the study. Both sexes were
reproductively active but no greeting or courtship behaviours were observed. Males on the focal study grid were
longer than females, and had shorter heads and longer tails, but were similar in colouration and skin filamentation.
The level of threat to H. capensis and our limited knowledge of its biology mean that further scientific study is
urgently needed to assist in developing sound management practices.
Introduction
Worldwide, seahorse populations are threatened by
(a) degradation of their estuarine, seagrass, mangrove
and coral habitats, (b) incidental capture in fishing gear
(bycatch), and (c) over-exploitation for use in traditional medicines, the aquarium trade and as curiosities.
Many species are experiencing population declines but
the conservation status of African species is unknown
(Vincent 1996). Seahorses are particularly vulnerable
to population decline because of their distinctive life
history, behaviour and ecology: they provide lengthy
and vital parental care for small broods, exhibit low
mobility and site-fidelity, have low natural rates of adult
36
mortality, and (in many species) maintain faithful pairbonds (reviewed in Lourie et al. 1999). In addition,
seahorses inhabit shallow, coastal areas worldwide,
where anthropogenic disturbances tend to be most
frequent and severe.
South Africa’s endemic Knysna Seahorse,
Hippocampus capensis Boulenger 1900, is the only
fully estuarine seahorse species among the 32 currently recognised (Lourie et al. 1999). It is also the
only seahorse species thus far inferred to be primarily at
risk from habitat damage (Whitfield 1995a, Day 1997,
Lockyear 19991 ). H. capensis has the smallest known
geographical range of any seahorse, inhabiting seagrass beds in only four estuaries on the southern coast
of South Africa: Knysna, Swartvlei, Keurbooms and
Klein Brak (Howard-Williamson & Allanson 1978,2
Kok 1981, Smith et al. 1986, Grindley 1985,3 Skelton
1987,4 Whitfield et al. 1983,5 Whitfield 1989a,b, 1995a,
Hanekom & Russell 1991,6 Russell 1994). Anecdotal
information suggests that H. capensis may also occupy
the Breede River, Duiwenhoks, Kaffirkuils and Groot
Brak (N. Grange, personal communication).
Human settlements and associated industrial,
domestic and recreational activities are increasing on
the shores of waters harbouring H. capensis. The
Knysna Estuary is among the most heavily used water
bodies in South Africa. Surrounding development is
known and inferred to have affected the estuarine
1
Lockyear, J. 1999. Proposal to Change the IUCN Red Listing
of Hippocampus capensis Boulenger 1990 (Knysna Seahorse).
Unpublished.
2
Howard-Williamson, C. & B.R. Allanson. 1978. Swartvlei
Project Report, Part II. The limnology of Swartvlei with special
reference to production and nutrient dynamics in the littoral zone.
Grahamstown. Institute for Freshwater Studies Special Report
No.78/3. 280 pp.
3
Grindley J.R. 1985. Report No. 30: Knysna (CMS 13). In:
A.E.F. Heydorn & J.R. Grindley (ed.) Estuaries of the Cape.
Part II: Synopses of available information on individual systems.
CSIR Research Report 429. 82 pp.
4
Skelton, P.H. 1987. Knysna Seahorse/Knysna-Seeperdjie.
South African Red Data Book – Fishes. South African National
Scientific Programmes Report 137: 93–95.
5
Whitfield, A.K., B.R. Allanson & T.J.E. Heinecken. 1983.
Report No. 22: Swartvlei (CMS 11). In: A.E.F. Heydorn &
J.R. Grindley (ed.) Estuaries of the Cape. Part II: Synopses
of available information on individual systems. CSIR Research
Report 421. 62 pp.
6
Hanekom, N. & I.A. Russell. 1991. The distribution and abundance of the Knysna seahorse, Hippocampus capensis Boulenger
1900, in the Knysna Estuary. National Parks Board of Trustees,
Internal Report (unpublished): 1–9.
ecosystem (Grindley & Eagle 1978, Plumstead 1990,
Whitfield 1995a) with trace metals, hydrocarbons,
pesticides and organic wastes among the identified
water pollutants (Chmelik 1975). However, information about the direct impact of these disturbances on
either estuarine habitats or their inhabitants is scarce
(Plumstead 1990).
H. capensis appears to be vulnerable to temperature
increases. In 1991, 3000 dead seahorses were found
along the shores of the Swartvlei Estuary after heavy
rainfall and flooding caused the breaching of the estuarine mouth and a sudden reduction in water level
(Russell 1994). Mortality was attributed to the resultant
increase in water temperature from the normal high of
28–32◦ C (Russell 1994).
H. capensis recently became the first seahorse
species to be listed as Endangered on the IUCN
Red List of Threatened Species because of its limited extent of occurrence and area of occupancy,
fragmented distribution, and ecosystem vulnerability
(Hilton-Taylor 2000). It is protected by the South
African Fisheries Act No. 58 (Grindley 19853 ), the
Marine Living Resources Act 1998 and the White
Paper for Sustainable Coastal Development in South
Africa (Mayekiso 20007 ). Further protection is offered
because the Knysna and Swartvlei estuaries are located
in the designated National Lakes Area (Skelton 19874 ).
Nonetheless, development around the estuary continues, with potentially considerable risk to H. capensis.
A dearth of information on H. capensis population
size, habitat requirements and population dynamics
severely limits management capacity (Skelton 1987,4
Day 1997). There are no published reports of in situ biological or ecological studies focusing on this species.
Most studies of H. capensis were conducted under captive conditions (Fourie 1997, Lockyear et al. 1997,
Tops 1999, Le Cheminant 2000) or examined their
genetics and morphology (Toeffie 2000). Only one
unpublished and limited study has considered their
population size (Hanekom & Russell 19916 ). Given
the species’ apparent vulnerability to ecological perturbations and the threat of habitat degradation, a better
understanding of the species’ basic ecology is imperative. This study provides preliminary baseline data on
H. capensis individuals and populations.
H. capensis is a medium-sized seahorse, with a
described adult height (presumably the top of the
7
Mayekiso, M. 2000. Report on the National Estuaries
Workshop, Port Elizabeth, 3–5 May 2000.
37
Figure 1. The Knysna Seahorse, H. capensis. Head length is measured from the tip of the snout to the mid-point of the cleithral
ridge: (a) trunk length is the distance from the cleithral ridge to
the lateral mid-point of the last trunk ring; (b) tail length is measured from the last trunk ring to the tip of the straightened tail.
Reproduced with permission of L. Richardson.
coronet to tip of the straightened tail) of 5.3–12.0 cm
(Smith 1981, Smith et al. 1986, Skelton 1987,4 Lourie
et al. 1999, Z. Toeffie in litt.). The species is characterised by a short snout, lack of coronet (Figure 1)
and males have a slight keel above the brood pouch.
Individuals are typically mottled brown with occasional darker patches, but are known to range in colour
from white through yellow, orange, green and beige, to
brown or black.
Evidence suggests that H. capensis reach sexual
maturity within 1 year of birth at approximately 6.5 cm
standard length (defined as the sum of the head, trunk
and tail lengths, Lourie et al. 1999, Whitfield 1995a).
They brood their young for 14–45 days (depending
on water temperature), and produce 7–120 young per
brood, each of which is 0.8–1.6 cm standard length
at birth (Grange & Cretchley 1995, Whitfield 1995a,
Lockyear et al. 1997). H. capensis can live for at least
3 years in captivity (Lockyear et al. 1997), but there are
no data on longevity in the wild.
H. capensis are found at depths of 0.5–20 m (Toeffie
2000) in submerged vegetation, and are known to
survive salinity changes from 1 to 59 ppt (Whitfield
1995a). In captivity, H. capensis are diurnally active
and have an elaborate courtship and mating ritual
involving brood pouch inflation, tail grasping and
‘face-to-face’ positioning (Grange & Cretchley 1995).
We expect H. capensis, like most seahorses, to move
slowly, ambush their prey, and rely on camouflage and
crypsis to avoid predation (Vincent 1990). They may
also form monogamous pair bonds as other seahorse
Figure 2. Map of the Knysna Estuary, South Africa. Dashed
lines = salt marshes; speckled area = intertidal mudflats;
closed circles = one or more transects surveyed. Modified from
Grindley 1985.3
species do (Dauwe 1992, Nijhoff 1993, Vincent 1995,
Vincent & Sadler 1995, Jones et al. 1998, Kvarnemo
et al. 2000, Perante et al. 2002).
Materials and methods
Study site
H. capensis were studied in the Knysna and surrounding estuaries (Figure 2). The Knysna (position
of mouth: 34◦ 04 35 S, 23◦ 03 40 E) is South Africa’s
largest permanent estuary (Grindley 19853 ). It is
approximately 21 km2 in area (Day 1981, Reddering &
Esterhuysen 19848 ) but extensive sandbanks mean that
the subtidal area covers only 10 km2 . Located at the
mouth of the 59-km long Knysna River (Grindley
19853 ), its 526 km2 catchment (Day 1981) includes
8
Reddering, J.S.V. & K. Esterhuysen. 1984. Sedimentation of
the Knysna Estuary. ROSIE Report No. 9. University of Port
Elizabeth, Department of Geography. 79 pp.
38
approximately 20 tributaries and streams (Grindley
19853 ). The estuary’s tidal reach is approximately
10 km (Reddering & Esterhuysen 19848 ). The maximum depth is 12 m below mean sea level, but the water
reaches a depth of greater than 16 m at the mouth of the
estuary (Day et al. 1952, Grindley 19853 ). The water
temperature varied between 14◦ C and 25◦ C (mean ±
s.d. = 20 ± 2◦ C) during our study, and horizontal
visibility ranged from less than 1–5 m.
H. capensis is one of approximately 200 species of
fish found in the estuary and is reported to inhabit beds
of Zostera capensis seagrass, the dominant aquatic
plant in the Knysna Estuary (Grindley 19853 ). The dry
biomass of Z. capensis in the estuary ranges from 68
to 238 g m−2 (Grindley 1976,9 Grindley & Snow 1983)
and it is most commonly found on shelving mud banks
at the low-water level of the spring tide, often in mixed
stands with Halophila ovalis (Grindley 19853 ). Above
the Westford Bridge (Figure 2), Z. capensis is gradually
replaced by Ruppia maritima (Grindley 19853 ).
Descriptions of the Swartvlei system (34◦ 00 S,
◦
23 46 E), the Keurbooms Estuary (34◦ 02 S, 23◦ 23 E)
and the Groot Brak Estuary (34◦ 06 S, 22◦ 09 E) can be
found in Whitfield et al. (1983),5 Duvenage & Morant
(1984)10 and Morant (1983),11 respectively.
Assessment of population parameters and
habitat occupancy
We conducted transect surveys to estimate the abundance of H. capensis in the Knysna Estuary, modifying
established techniques for the rapid assessment of fish
abundance (Ginsburg et al. 199812 ). Transect counts
are well suited to sedentary species such as seahorses (Buxton & Smale 1989). A team of four divers
spent 10 days familiarising themselves with estuarine
9
Grindley, J.R. 1976. Report on the ecology of Knysna Estuary
and proposed Braamekraal Marina. University of Cape Town,
School of Environmental Studies. 123 pp.
10
Duvenage, I.R. & P.D. Morant. 1984. Report No. 31:
Keurbooms/Bitou System (CMS 19), Piesang (CMS 18). In:
A.E.F. Heydorn & J.R. Grindley (ed.) Estuaries of the Cape.
Part II: Synopses of available information on individual systems.
CSIR Research Report 430. 64 pp.
11
Morant, P.D. 1983. Report No. 20: Groot Brak (CMS 3).
In: A.E.F. Heydorn & J.R. Grindley (ed.) Estuaries of the Cape.
Part II: Synopses of available information on individual systems.
CSIR Research Report 429.
12
Ginsburg, R.N., P. Kramer, J. Lang, P. Sale & R. Steneck.
1998. Atlantic and Gulf Reef Assessment (AGRRA) Revised
Rapid Assessment Protocol (RAP).
diving conditions, developing survey techniques, and
forming a search image for H. capensis before data
collection began. Exploratory dives were also undertaken in Swartvlei Estuary, Swartvlei Lake, Keurbooms
Estuary, Groot Brak and Klein Brak.
We conducted 82 transect surveys throughout the
Knysna Estuary from 23 February to 4 April 2000, surveying a total of 4920 m2 (82 transects, 30 m long×2 m
wide). The GPS grid map of the Knysna Estuary was
marked into 31 1-km2 grid squares, each surveyed at
least once during the study period. The origin and direction of the transects were randomly chosen within each
grid square. The number of transects per grid square,
which varied from 1 to 5, was determined by available
time and accessibility.
Before entering the water, GPS location, transect
bearing, weather, and water conditions were recorded.
Pairs of divers swam the transect together on SCUBA,
with the divers searching adjacent 1 m wide swaths
as they reeled out a 30 m rope, fixed at the origin. Whenever a seahorse was located, one diver
noted its location along the transect, depth, habitat
type (Table 1), holdfast, sex, maturity, reproductive
state, colour, the presence and length of filamentous
appendages, and distinguishing features. The second
diver used a plastic ruler marked in cm and mm to
measure its head, trunk and tail lengths. Previous studies have used various metrics to describe H. capensis.
We standardised our measurements according to Lourie
et al. (1999) (Figure 1). Sex was determined by the
presence (male) or absence (female) of a brood pouch.
Table 1. Habitat categories employed in estimate of seahorse
density and abundance.
Category
Description
Bare
Zostera capensis
Total vegetation cover ≤2%
Only species present or proportion of this
species exceeds the proportion of other
vegetation types by ≥10%
Only species present or proportion of this
species exceeds the proportion of other
vegetation types by ≥10%
Only species present or proportion of this
species exceeds the proportion of other
vegetation types by ≥10%
≥2 species present in proportions that
differ by <10%
<20% substrate covered with vegetation
20–40% substrate covered with
vegetation
>40% substrate covered with vegetation
Caulerpa filiformis
Halophila ovalis
Mixed
Low density
Medium density
High density
39
Small seahorses (below the 7.1 cm standard length
at which we first observed pouches) were recorded
as juvenile but may have been young females. We
also noted whether males were pregnant or not pregnant. Female reproductive state is commonly defined
by whether her trunk shape indicates that she is
holding hydrated eggs or has just transferred eggs
(Vincent & Sadler 1995, Perante et al. 2002), but we
found this too difficult to determine with accuracy in
H. capensis.
The divers fixed the rope at the end of the transect
and returned along the line, each noting habitat and
vegetation type, percentage cover, vegetation height,
sediment composition, slope, depth, topographical features and associated species of invertebrates (e.g. the
stinging cnidarian, Tubularia warreni) and fish within
two 1 m2 quadrats at 5 m intervals. Water temperature
readings were taken underwater at the start and end
point of each transect, and current strength and visibility were also noted. Transect lines were removed after
the return swim.
Spatial patterns and social behaviour
We undertook a brief second study in order to document H. capensis movement and behaviour in a small
and apparently densely populated part of the Knysna
Estuary, following the protocol of Vincent & Sadler
(1995). We used plastic tent pegs and photodegradable
flagging tape to lay down a 10 m × 10 m grid (with
2 m × 2 m grid squares), hereafter referred to as the
focal study grid, at the Laguna Grove jetty (Figure 2).
We then monitored seahorses on 10 mornings between
13 March and 4 April 2000.
Seahorses located within the focal study grid were
tagged using numbered, green, plastic tags (approximately 4 mm × 2 mm), hung loosely around the neck
of the seahorse with cotton thread. Such individual tagging is necessary for identification because seahorses
can change colour and dermal appendages can be lost
(Vincent 1990, Vincent & Sadler 1995). As we tagged
each seahorse, we recorded its position on the focal
study grid, holdfast, colour, sex, reproductive state,
filaments on the body (percentage cover and length),
head length, trunk length, tail length, distance to the
nearest known neighbour, and the sex and reproductive state of the neighbouring seahorse. We monitored
the tagged animals closely during our study, loosening or cleaning their tags as necessary. Tags were not
removed at the end of our study as a colleague tracked
them for further research. They were removed once the
subsequent study was completed.
The study site was visited daily when weather conditions and visibility permitted. Two divers swam over
the focal study grid systematically searching each 4-m2
grid square for seahorses and tagging any new animals.
When a tagged animal was resighted, the divers would
briefly float a minimum of 1 m away from the seahorse
and note its tag number, position on the focal study
grid, and behaviour (as per Vincent 1990).
Analysis of seahorse spatial patterns on the focal
study grid was conducted using Minimum Convex
Polygons (MCPs), a robust technique for use in short
studies such as ours where very few recapture positions (fixes) are available per animal (Harris et al.
1990). The method calculates the area of the polygon
that connects the outermost fixes for each animal. We
calculated the MCP area occupied during the study
and polygon length (the maximum distance between
two corners of each polygon) for each seahorse, using
Wildtrak version 1.2, a non-parametric home range
analysis program (Todd 199213 ). The MCP area and
length data were logarithmically transformed to normalise distributions, then analysed using Student’s
t-tests. All means are reported with standard deviation
unless otherwise stated.
Results
We found a total of 44 seahorses in the 82 transects,
with 18 transects yielding one or more seahorses. In
addition, we tagged and studied 91 seahorses on the
focal study grid. Not all data are available for each of
the seahorses observed in the Knysna Estuary. Of the
other water bodies surveyed, we found H. capensis in
only the Swartvlei Estuary (Table 2).
Population parameters
Observed seahorse densities in the randomly distributed
transects ranged from 0 to 0.25 m−2 , with a mean overall density of 0.0089 m−2 (Figure 3). Extrapolating
from our transects to the total 10 km2 subtidal
area of the Knysna Estuary yielded a population
13
Todd, I.A. 1992. Wildtrak: Non-parametric home range analysis for Macintosh computers (Version 1.2). Department of
Zoology, University of Oxford, U.K. Current address: University
of Hertfordshire, UK.
40
Table 2. Number of H. capensis found and effort allocated to
searching in the Knysna Estuary and surrounding water bodies.
Table 3. Numbers of male, female and juvenile H. capensis found
in the Knysna Estuary.
Water body Number of No. sites Estuarine Person-hours∗
spent
seahorses surveyed area
surveying
found
(km2 )
Females Males Males : Total Juveniles Total
adults
Knysna
44
Swartvlei
19
Swartvlei
0
Lake
Keurbooms 0
Groot Brak
0
Klein Brak
0
82
6
2
29
4
3
10.01§
2.02
8.82
c. 3.03
0.54
164
24
4
12
7
3
Focal study 47
grid
Transect
12
survey
Total
59
44
0.484
0
91
29
0.707∗
3
44
73
0.553
3
135
∗
Indicates significantly biased sex ratio (chi-square test,
p < 0.05).
= Duration of survey in hours multiplied by the number of
people on the survey team. § = Subtidal area. 1 = Grindley
(1985)3 . 2 = Whitfield et al. (1983)5 . 3 = Duvenage & Morant
(1984)10 . 4 = Morant (1983)11 .
∗
Figure 3. Density of H. capensis observed in all transects, in
transects of habitat types defined in Table 1, and in different
densities of vegetation. Values are mean ± bootstrapped 95%
confidence intervals of the mean. No transects were dominated by
H. ovalis.
estimate of approximately 89 000 seahorses, with
a bootstrapped (Efron & LePage 1992, Efron &
Tibshirani 1993) 95% confidence interval of 30 000–
148 000 animals. The mean density of seahorses
observed on the focal study grid over all days was
0.22 m−2 , but density ranged from 0.04 to 0.46 m−2 .
Mature animals accounted for 93% of the observed
population in the transects (with just three juveniles)
and all of the seahorses on the focal study grid.
Significantly more males than females were observed
during the transect surveys (χ 2 = 7.05, n = 41, p =
0.008; Table 3). However, no sex ratio bias was found
Figure 4. Relationship between seahorse density and total vegetation cover in the 82 transects. Each open circle represents one
transect.
among the seahorses on the focal study grid (χ 2 =
0.099, n = 91, p = 0.753; Table 3).
Habitat occupancy
Seahorse density in the transects was not significantly
correlated with percent cover of Z. capensis, Caulerpa
filiformis, H. ovalis, total vegetation cover, depth, or
T. warreni density (Spearman rank order correlation:
rs < 0.144, n = 82, p > 0.200 for all habitat parameters; Figure 4). However, when we broke vegetation
density into categories we found that H. capensis
were most commonly associated with relatively sparse
(i.e. ≤20% cover) vegetation (Figures 3 and 4): such
habitats accounted for only 60% of the area surveyed
41
but contained 82% of the seahorses we observed (χ 2 =
8.27, n = 44; p = 0.004). A holdfast choice was available in all of the 18 transects in which seahorses were
observed. However, H. capensis were most likely to be
found grasping Z. capensis holdfasts (χ 2 > 10.0, n =
41, p < 0.001). Zostera capensis accounted for 51% of
available holdfasts, but 76% of seahorses were found
grasping this seagrass.
Spatial behaviour
A total of 62% (57 of 91) of the seahorses on the focal
study grid were resighted after tagging, on 1–5 subsequent days during the 10 days that we monitored them.
Total fixes per resighted animal ranged from 2 to 6
(mean = 3.8 ± 1.1 fixes), with the last resighting a
mean of 6.8 ± 3.7 days after tagging. Male and female
H. capensis were resighted with approximately equal
frequency (t29 = 0.466, p = 0.645).
Movement patterns were analysed only for the
31 seahorses for which we had at least three fixes.
We found no difference between the sizes of the areas
over which males and females were resighted (t29 =
0.078, p = 0.938; Table 4), or the length of these areas
(t29 = 0.976, p = 0.337; Table 4).
Social behaviour
H. capensis seahorses in the Knysna Estuary were
reproductively active, with 77% of all males brooding embryos at some point during the study: this
included 62% of the males (n = 18) in the transects
and 86% of the males (n = 38) on the focal study
grid. However, we observed no apparent greeting or
courtship behaviours.
No obvious social groupings were noticed during our
research. The maximum number of seahorses present
on the focal study grid on any one day was 46, a density
of 0.46 m−2 , on 24 March 2000 (Figure 5). The mean
known distance to the nearest neighbour was 61±35 cm
(n = 43 seahorses), with a range of 0 to 143 cm. The
nearest neighbour was equally likely to be of the same
or the opposite sex (χ 2 = 0.37, p = 0.542). We noted
a total of 21 occurrences of two neighbouring animals
less than 50 cm apart from one other, the distance at
which they could be assumed to be aware of one another
in a similar seagrass habitat with low-horizontal visibility (Vincent & Sadler 1995): none were male–male
combinations. Only 10 of these pairs of two animals
were close enough (two mean body lengths; approximately 33 cm) that physical contact might have been
possible. Most (60%) included one member of each
sex, while the rest included two females.
Sexual dimorphism
Males were longer than females on the focal study grid
(t86 = 1.86, p = 0.067), and had longer tails (t86 =
3.05, p = 0.003; Figure 6a) and shorter heads (t86 =
2.37, p = 0.020) than females, although trunk lengths
were not different (t86 = 1.18, p = 0.241). When
we controlled for standard length by including it as
a covariate in an ANCOVA, small females on the focal
study grid had proportionately shorter trunks (sex–
standard length interaction: F1,84 = 6.83, p = 0.011;
Figure 6b) and longer tails (sex–standard length interaction: F1,84 = 5.60, p = 0.020) than similar-sized
males, while large females had proportionately longer
Table 4. Minimum Convex Polygon areas of resighting, and their
lengths, on the focal study grid.
Females
MCP area of resighting (n = 16)
Mean
2.0 m2
SE
0.4 m2
Range
0.1–11.8 m2
Length of area of resighting (n = 15)
Mean
3.3 m
SE
0.2 m
Range
1.5–6.5 m
Males
1.5 m2
0.4 m2
0.2–6.2 m2
3.0 m
0.5 m
0.8–7.5 m
Figure 5. Seahorse positions on the focal study grid on 24 March
2000. Open diamonds = females; filled squares = males; filled
diamond = two females; open circle = one male and one female.
42
Figure 6. Seahorse morphometrics for the focal study grid:
(a) mean (±95% confidence interval) standard length (diamonds),
trunk length (circles), tail length (triangles), and head length
(squares) for males (open symbols) and females (filled symbols).
∗
indicates a significant difference between males and females;
(b) trunk (circles) and tail (triangles) lengths as a function of
standard length, for males and females. The lines are regressions
for each sex, and the slopes differ significantly between the sexes
for each metric.
trunks and shorter tails. There were not enough animals
in the transect study to conduct a proper dimorphism
analysis.
Seahorse colour and adornment did not differ clearly
by sex, but 87% of males observed throughout the
estuary were darkly coloured (black, brown, grey,
green) as compared with 61% of females. In addition,
all black seahorses were males (n = 7) and all orange
or white seahorses were females (n = 10). Dark spots
or mottling were observed on 43% of individuals and
39% had skin filaments while the rest were smooth.
Filaments were generally found dorsally and measured
0.5–5.0 mm long (mean = 2.2 ± 1.0 mm, n = 130).
Discussion
Population parameters
This first published field study of H. capensis abundance and distribution takes on particular importance because the species’ entire area of occupancy
probably measures less than 50 km2 (Lockyear
1999,1 Hilton-Taylor 2000). Our brief surveys found
H. capensis in only the Knysna and Swartvlei estuaries, with the former having by far the larger population.
Few person hours were spent outside the Knysna, however, and heavy rains led to very poor visibility in the
Groot Brak and Klein Brak estuaries.
Our population estimate of 89 000 adult H. capensis
in the Knysna Estuary is higher than the 23 000
derived from a very limited seine net survey
(Hanekom & Russell 19916 ), and must be used very
tentatively. Further investigations (including markrecapture studies) are urgently needed in the Knysna
and surrounding estuaries in order to obtain a more reliable estimate. Our transects were randomly stratified
throughout the estuary but covered only a small proportion of the total area. We found seahorses in only 22%
of the 82 transects. The habitat preferences we report
in this paper should allow future assessments to stratify
sampling by vegetation cover and estimate population
abundance more precisely based on the proportion of
‘preferred’ habitat available.
The mean density of H. capensis on our densely populated focal study grid (mean density = 0.22 m−2 )
was roughly the same as densities of unexploited
Australian temperate seahorse species on similar
study grids (0.080–0.215 m−2 : Vincent et al. submitted manuscript14 ; 0.162 m−2 : M.-A. Moreau unpublished data) but higher than those for an exploited
seahorse population on coral reefs (0.019 m−2 : Perante
et al. 2002) or a temperate pipefish in seagrasses
(0.02–0.10 m−2 : Bayer 1980).
The dearth of juvenile H. capensis observed in
the Knysna Estuary corroborates the findings of previous research, in which no seahorse smaller than
5.1 cm standard length was found (P. Joubert personal
communication), and is typical of seahorse population assessments (see above studies, K. Martin-Smith,
unpublished data). Very young H. capensis may be
spending time in the plankton, at least initially: channel nets deployed to catch ichthyoplankton in the
Swartvlei Estuary yielded a net movement of 4 091
post-larval, juvenile seahorses out of the estuary mouth
in October 1986 and a net movement into the estuary of
250 in November 1986, over a 24-h period (Whitfield
1989a). Older juvenile H. capensis may subsequently
use different habitats from adults, a behavioural pattern
observed in other species. For example, H. comes juveniles were found predominantly in Sargassum whereas
adults used coral and sponge holdfasts (Perante et al.
1998).
Sex ratios appear variable in syngnathids. The
preponderance of male H. capensis in our transect
14
Vincent, A.C.J., K.L. Evans & A.D. Marsden. Home range
behaviour of the monogamous Australian seahorse, Hippocampus
whitei. Anim. Behav., submitted manuscript.
43
surveys contrasted with findings for H. comes (Perante
et al. 1998) and H. zosterae (Strawn 1958) and
some populations of H. abdominalis (K. Martin-Smith
unpublished data), where females outnumbered males.
However, the lack of sex-ratio bias observed on
our H. capensis focal study grid was consistent
with comparable studies of H. whitei (Vincent &
Sadler 1995) and H. breviceps (M.-A. Moreau unpublished data). In contrast, sex ratios of a pipefish,
Corythoichthys haematopterus, were female biased in
Japan (Matsumoto & Yanagisawa 2001).
Habitat occupancy
The dearth of correlations between the density of
H. capensis and vegetation or depth in our transects
runs contrary to previously-noted associations between
H. capensis and Z. capensis (Skelton 1987,4 Whitfield
et al. 1989, Whitfield 1995a). We did, however, find
that H. capensis tended to use Z. capensis holdfasts
preferentially, so it may be that previous work had
focused on smaller-scale assessments. Other species
of seahorses have been recognised as preferentially
associating with particular seagrasses, such as the
Australian H. whitei with Posidonia sp. (Middleton
et al. 1984) or with mixed Posidonia australis and
Z. capricorni (Vincent et al. submitted manuscript14 ).
The basis for such habitat associations is not understood, and could be a matter of post-settlement choice,
an outcome of settlement patterns based on other
parameters, or differential mortality (Kramer et al.
1997).
The high density of H. capensis observed in low
density vegetation stands (≤20% total cover) is probably a genuine distribution pattern, given the slow
and careful search we undertook in dense vegetation areas and the fact that we were able to discover
seahorses in very dense vegetation in the Swartvlei
Estuary. Prey abundance and opportunities for crypsis
are usually considered to be greater in denser vegetation (Bell & Westoby 1986, Ansari et al. 1991) but
water exchange and some feeding opportunities may
be greater in less dense vegetation. Other seahorse
species are certainly also found in sparse vegetation
for at least some activities (M.-A. Moreau unpublished
data, Vincent & Sadler 1995), while some are found on
bare soft bottoms (K. Martin-Smith unpublished data).
H. capensis is also reported to sometimes rest on bare
sediment or in shrimp burrows (N. Grange personal
communication).
Spatial and social behaviour
Most seahorses in our study exhibited some spatial
fidelity to an area, with nearly two-thirds resighted at
least once after tagging and within 7 days of their first
sighting. Since tagged seahorses were not resighted
every day, they probably ranged beyond the perimeter of our 100 m2 focal study grid. Our focal study
was too brief and small-scale to determine whether
H. capensis maintained small home ranges as some
species do (Perante et al. 2002, Vincent et al. submitted manuscript,14 J. Anticamara unpublished data), or
ranged more widely as in others (J. Curtis unpublished
data, K. Martin-Smith unpublished data).
A large proportion of H. capensis in the Knysna
Estuary were reproductively active. H. capensis has
been reported to breed in the austral summer when
water temperatures approach 20◦ C (Whitfield 1995a,
Grange & Cretchley 1995, Fourie 1997, P. Joubert
personal communication), which would put our study
near the end of the season, consistent with the lack
of observed courtship behaviours. There is, however,
some evidence of breeding in the wild throughout the
year (J.-.P. Arabonis personal communication) and that
breeding season can be extended in captivity with
photo-thermal manipulation (Lockyear et al. 1997).
The lack of observed male–male encounters will need
to be investigated further in light of research on other
seahorse species showing that males compete more
actively than females for access to mates (Vincent 1994,
Masonjones & Lewis 1996) and earlier evidence of
male competition in H. capensis (Fourie 1997).
Sexual dimorphism
The greater male standard length for H. capensis on
the focal study grid is unusual in seahorses. A similar situation has been observed in H. spinosissimus
and H. trimaculatus (J. Meeuwig unpublished data)
but dimorphism was not found in studies on nine
other species, although males frequently had longer
tails than females and females had longer trunks than
males (Vincent 1990, K. Martin-Smith unpublished
data, M.-A. Moreau unpublished data). In general,
longer male tails have been explained by their role
in mate competition (males of some species wrestle
with their tails: Vincent 1994), parental care (location
of the brood pouch), and movement (anchoring the
male with his heavy brood) (Vincent 1990, Vincent
1994, Fourie 1997). A similar situation is reported to
44
exist in the pipefish, Syngnathus typhle (Berglund et al.
1986).
Conservation implications
The majority of all known H. capensis are found in
the Knysna Estuary, where the species’ apparent vulnerability to environmental change in parameters such
as temperature (Russell 1994) is part of the reason for
its IUCN Red Listing as Endangered (Hilton-Taylor
2000). This species is heterogeneously distributed, with
seahorses in only 22% of transects and a disproportionately high concentration observed at the site chosen for
our focal study grid.
Development along the shores of the Knysna will
need to proceed cautiously, with comprehensive and
focused environmental impact assessments. Significant
concentrations of H. capensis will require particularly
careful management measures. In addition, it will be
important to retain the low density (≤20% total cover)
vegetation stands and Z. capensis holdfasts that appear
to be the ‘preferred’ seahorse habitat in the Knysna
Estuary.
The Endangered status of H. capensis should preclude exploitation of these seahorses, whether wild or
captive. Aquaculture ventures could pose significant
threats to wild H. capensis: poor aquaculture practices
often damage the marine environment and disrupt wild
populations of the farmed species and others (Naylor
et al. 2000). In particular, releases of captive-bred
H. capensis could damage populations of wild seahorses by carrying disease, altering genetics and/or
disrupting social and spatial behaviour (IUCN 1995).
Any plans to culture H. capensis will need thorough
environmental assessment.
The threats to H. capensis are real. A closely related
South African, estuarine pipefish species, Syngnathus
watermeyeri, was considered to be a very rare example
of an estuarine fish that had gone extinct (Groombridge
1993, Whitfield 1995b). It was re-discovered in 1995
in one estuary (East Kleinemonde), and there is a tiny
remnant population in a second (Bushmans) (P. Cowley
in litt.). Biologists moved 12 pipefish to the West
Kleinemonde Estuary in 1997 and the population
appears to be viable to this point in time (P. Cowley
in litt., 19 November 2001, Cowley & Whitfield
2001). Releases must not, however, be contemplated
in the case of H. capensis at present: supplementations and translocations carry so many risks (IUCN
1995) that they should only be considered if all other
conservation approaches fail, as a last (and unreliable)
resort.
Substantially more research on the basic life history
and ecology of H. capensis will help to secure its future
and new approaches, such as molecular and genetic
research, may be of use in clarifying the population
structure and genotypic health of seahorse populations.
The utility of any biological research will, however,
depend on the value that decision-makers and stakeholders in the Knysna Estuary put on retaining healthy
populations of this Endangered fish.
Acknowledgements
This is a contribution from Project Seahorse. The
field study was funded by the John G. Shedd Aquarium, Chicago, U.S.A. A.D. Marsden was supported
by Guylian Chocolates of Belgium. Project Seahorse
gratefully acknowledges the help, enthusiasm and
advice offered by many colleagues and supporters in
South Africa. Particular thanks to P. Joubert, R. Milne
and the entire South African National Parks staff
in Knysna and Swartvlei for their logistic assistance and expertise; P. Teske, Stellenbosch University
for assistance with the transect surveys and focal
study; C. & P. Mulder, Thesen Islands Development
Company, for their hospitality; A. Boyd, C. Attwood &
S. Lamberth, Department of Sea Fisheries, A. Heydorn, environmental consultant, and N. Grange for
their support and advice. We thank K. Martin-Smith,
M.-A. Moreau, J. Curtis, J. Meeuwig and two anonymous referees for their constructive input to the
manuscript.
References cited
Ansari, Z.A., C.U. Rivonker, P. Ramani & A.H. Parulekar. 1991.
Seagrass habitat complexity and macroinvertebrate abundance
in Lakshadweep coral reef lagoons, Arabian Sea. Coral Reefs
10: 127–131.
Bayer, R.D. 1980. Size, seasonality, and sex ratios of the Bay
Pipefish (Syngnathus leptorhynchus) in Oregon. Northwest Sci.
54: 161–166.
Bell, J.D. & M. Westoby. 1986. Abundance of macrofauna in
dense seagrass is due to habitat preference, not predation.
Oecologia 68: 205–209.
Berglund, A.G., G. Rosenqvist & I. Svensson. 1986. Reversed
sex roles and parental energy investment in zygotes of two
pipefish (Syngnathidae) species. Mar. Ecol. Prog. Ser. 29:
209–215.
Buxton, C.D. & M.J. Smale. 1989. Abundance and distribution patterns of three temperate marine reef fish
45
(Teleostei: Sparidae) in exploited and unexploited areas off the
Southern Cape coast. J. Appl. Ecol. 26: 441–451.
Chmelik, F.B. 1975. Economic model for estuarine evaluation. Pretoria Department of Planning and the Environment
Bulletin 2. 105 pp.
Cowley, P.D. & A.K. Whitfield. 2001. Ichthyofaunal characteristics of a typical temporarily open/closed estuary on the
southeast coast of South Africa. Ichthyol. Bull. J.L.B. Smith
Inst. Ichthyol. 71: 1–19.
Dauwe, B. 1992. Ecologie van het zeepaardje Hippocampus reidi
(Syngnathidae) op het koraalrif van Bonaire (N.A.): Habitatgebruik, reproductie en interspecifieke interacties. (Ecology
of the seahorse Hippocampus reidi on the coral reefs of
Bonaire (N.A.): habitat use, reproduction and interspecific
interactions.). M.Sc. Thesis, Rijksuniversiteit Groningen,
the Netherlands. 65 pp.
Day, D.H. (ed.) 1981. Estuarine ecology with particular reference
to South African estuaries. Balkema, Cape Town. 411 pp.
Day, L. 1997. Drifting into danger: Seahorses. Africa – Environment and Wildlife 5: 66–71.
Day, J.H., N.A.H. Millard & A.D. Harrison. 1952. The ecology of
South African estuaries. Part III Knysna: A clear open estuary.
T. Roy. Soc. S. Afr. 33: 367–413.
Efron, B. & R. LePage. 1992. Introduction to bootstrap. pp. 3–10.
In: R. LePage and L. Billard (ed.) Exploring the Limits of
Bootstrap, John Wiley & Sons, New York.
Efron, B. & R.J. Tibshirani. 1993. An introduction to the
bootstrap. Chapman & Hall, New York. 436 pp.
Fourie, D. 1997. Sex-roles and the influence of size on mating
competition in the Knysna seahorse, Hippocampus capensis.
Honours Thesis, University of Stellenbosch. 15 pp.
Grange, N. & R. Cretchley. 1995. A preliminary investigation of the reproductive behaviour of the Knysna seahorses,
Hippocampus capensis Boulenger 1900. S. Afr. J. Aquat. Sci.
21: 103–104.
Grindley, J.R. & G.A. Eagle. 1978. Environmental effects of the
discharge of sewage effluent into Knysna Estuary. University
of Cape Town, School of Environmental Studies. 62 pp.
Grindley, J.R. & C.S. Snow. 1983. Environmental effects of the
discharge of sewage effluent into Knysna Lagoon. University
of Cape Town, School of Environmental Studies. 55 pp.
Groombridge, B. (ed.) 1993. 1994 IUCN Red List of Threatened
Animals. IUCN, Gland. 286 pp.
Harris, S., W.J. Cresswell, P.G. Forde, W.J. Trewhella,
T. Woollard & S. Wray. 1990. Home-range analysis using
radio-tracking data – a review of the problems and techniques
particularly as applied to the study of mammals. Mammal Rev.
20: 97–123.
Hilton-Taylor, C. (compiler) 2000. 2000 IUCN Red List
of Threatened Species. IUCN/SSC, Gland, Switzerland &
Cambridge, U.K. http://www.redlist.org.
IUCN. 1995. Guidelines for re-introductions. Gland, Switzerland.
http://www.iucn.org.
Jones, A.G., C. Kvarnemo, G.I. Moore, L.W. Simmons &
J.C. Avise. 1998. Microsatellite evidence for monogamy and
sex-biased recombination in the Western Australian seahorse
Hippocampus angustus. Mol. Ecol. 7: 1497–1505.
Kok, H.M. 1981. Knysna seahorse distribution poses a problem.
African Wildlife 35: 9.
Kramer, D.L., R.W. Rangeley & L.J. Chapman. 1997. Habitat
selection: Patterns of spatial distribution from behavioural decisions. pp. 37–80. In: J.-G.J. Godin (ed.) Behavioural Ecology
of Teleost Fishes. Oxford University Press.
Kvarnemo, C., G.I. Moore, A.G. Jones, W.S. Nelson & J.C. Avise.
2000. Monogamous pair bonds and mate switching in the
Western Australian seahorse Hippocampus subelongatus.
J. Evol. Biol. 13: 882–888.
Le Cheminant, J. 2000. An investigation to establish the suitability
of Opalithplattchen (Bee Tag), Fly and Visible Implant Fluorescent Elastomer (VIFE) tagging systems for marking the Knysna
seahorse, Hippocampus capensis. M.Sc. thesis, Bournemouth
University. 83 pp.
Lockyear, J.F., H. Kaiser & T. Hecht. 1997. Studies on the captive breeding of the Knysna Seahorse (Hippocampus capensis).
Aquar. Sci. Conserv. 1: 129–136.
Lourie, S.A., A.C.J. Vincent & H.J. Hall. 1999. Seahorses: An
identification guide to the world’s species and their conservation. London, U.K. 214 pp.
Masonjones, H.D. & S.M. Lewis. 1996. Courtship behavior
in the dwarf seahorse, Hippocampus zosterae. Copeia 3:
634–640.
Matsumoto, K. & Y. Yanagisawa. 2001. Monogamy and sex role
reversal in the pipefish Corythoichthys haematopterus. Anim.
Behav. 61: 163–170.
Middleton, M.J., J.D. Bell, J.J. Burchmore, D.A. Pollard &
B.C. Pease. 1984. Structural differences in the fish communities of Zostera capricorni and Posidonia australia seagrass
meadows in Botany Bay, New South Wales. Aquat. Bot. 18:
89–109.
Naylor, R.L., R.J. Goldburg, J.H. Primavera, N. Kautsky,
M.C.M. Beveridge, J. Clay, C. Folke, J. Lubchenco,
H. Mooney & M. Troell. 2000. Effect of aquaculture on world
fish supplies. Nature 405: 1017–1024.
Nijhoff, M. (1993) Voortplantingsecologie van het zeepaardje
Hippocampus reidi op het koraalrif van Bonaire. (Reproductive ecology of the seahorse Hippocampus reidi on a
Bonaire coral reef.). M.Sc. thesis, Rijksuniversiteit Groningen,
the Netherlands. 49 pp.
Perante, N.C., M.G. Pajaro & A.C.J. Vincent. 1998. Demographics of the seahorse Hippocampus comes in the Central
Philippines. pp. 439–448. In: B. Morton (ed.) The Marine
Biology of the South China Sea. Proceedings of the Third
International Conference on the Marine Biology of the South
China Sea, Hong Kong, 28 October–1 November, 1996. Hong
Kong University Press.
Perante, N.C., M.G. Pajaro & A.C.J. Vincent. 2002. Biology
of a seahorse species, Hippocampus comes, in the central
Philippines. J. Fish Biol. 60: 821–837.
Plumstead, E.E. 1990. Changes in ichthyofaunal diversity and
abundance within the Mbashe Estuary, Transkei, following construction of a river barrage. S. Afr. J. Mar. Sci. 9:
399–407.
Russell, I.A. 1994. Mass mortality of marine and estuarine fish
in the Swartvlei and Wilderness Lake systems, Southern Cape.
S. Afr. J. Aquat. Sci. 20: 93–96.
Smith, M.M. 1981. The Seahorse of the Knysna Lagoon. African
Wildlife 35: 6–9.
46
Smith, M.M., P.C. Heemstra & J.L.B. Smith (ed.) 1986. Smith’s
Sea Fishes, 6th edn. Springer-Verlag, Berlin. 1047 pp.
Strawn, K. 1958. Life history of the pigmy seahorse,
Hippocampus zosterae Jordan and Gilbert, at Cedar Key,
Florida. Copeia 1958: 16–22.
Toeffie, Z. 2000. A preliminary examination of the morphology and genetic structure within populations of the Knysna
seahorse, Hippocampus capensis (Pisces: Syngnathidae), from
two South African estuaries. M.Sc. thesis, University of the
Western Cape. 102 pp.
Tops, S. 1999. An investigation into the effects of habitat
complexity and food types on the behaviour of the Knysna
Seahorse – Hippocampus capensis. Honours Thesis, University
of St. Andrews. 53 pp.
Vincent, A.C.J. 1990. Reproductive ecology of seahorses.
Ph.D. Thesis, University of Cambridge. 109 pp.
Vincent, A.C.J. 1994. Seahorses exhibit conventional sex roles in
mating competition, despite male pregnancy. Behaviour 128:
135–151.
Vincent, A.C.J. 1995. A role for daily greetings in maintaining
seahorse pair bonds. Anim. Behav. 49: 258–260.
Vincent, A.C.J. 1996. The International Trade in Seahorses.
TRAFFIC International, Cambridge, UK. 163 pp.
Vincent, A.C.J. & L.M. Sadler. 1995. Faithful pair bonds in wild
seahorses, Hippocampus whitei. Anim. Behav. 50: 1557–1569.
Whitfield, A.K. 1989a. Ichthyoplankton interchange in the mouth
region of a southern African estuary. Mar. Ecol. Prog. Ser. 54:
25–33.
Whitfield, A.K. 1989b. Fish larval composition, abundance and
seasonality in a southern African estuarine lake. S. Afr. J. Zool.
24: 217–224.
Whitfield, A.K. 1995a. Threatened fishes of the world:
Hippocampus capensis Boulenger 1900 (Syngnathidae).
Environ. Biol. Fish. 44: 362.
Whitfield, A.K. 1995b. Threatened fishes of the world:
Syngnathus watermeyeri Smith, 1963 (Syngnathidae) Environ.
Biol. Fish. 43(2): 152.
Whitfield, A.K., L.E. Beckley, B.A. Bennett, G.M. Branch,
H.M. Kok, I.C. Potter & R.P. Van der Elst. 1989. Composition,
species richness and similarity of ichthyofaunas in eelgrass,
Zostera capensis, beds of Southern Africa. S. Afr. J. Mar. Sci.
8: 251–259.