Biol Invasions (2011) 13:2997–3003
DOI 10.1007/s10530-011-9984-z
ORIGINAL PAPER
Are botanical gardens a risk for zooplankton invasions?
Ian C. Duggan • Kathryn S. Duggan
Received: 29 November 2010 / Accepted: 10 March 2011 / Published online: 23 March 2011
Ó Springer Science+Business Media B.V. 2011
Abstract A number of zooplankton invasions have
been linked with the movement of plants to botanical
and other public gardens. Although most of these
records are historical, several recent examples indicate
that aquatic fauna may still be transported by plant
movements among gardens, or that there are unrec-
ognised long-standing established populations in gar-
den ponds around the world. We sampled 40 ponds
from 10 gardens, in the United Kingdom and United
States, to determine whether there is a high prevalence
of non-indigenous zooplankton in garden ponds that
could spread more widely if provided opportunity. No
non-indigenous species were recorded from any of
the gardens visited. We conclude that most well-
established gardens do not pose a major threat for
zooplankton invasions, mainly due to the destruction of
ponds and associated populations through time, which
apparently occurs commonly. In addition, ponds are
regularly cleaned, insecticides are used on plants
that may enter the water, and small fish are fre-
quently added to conservatory ponds, further reducing
the probability of zooplankton survival. Extirpation
of populations may be occurring at a greater rate
than re-introduction, due to greater restrictions on
I. C. Duggan (&)
K. S. Duggan
Department of Biological Sciences, Centre
for Biodiversity and Ecology Research, The University
of Waikato, Private Bag 3105, Hamilton, New Zealand
e-mail: i.duggan@waikato.ac.nz
movement of plants, while the increasing focus on ex-
situ conservation and science rather than aesthetics by
botanical gardens means that fewer aquatic plants are
being moved.
Keywords Botanical gardens
Craspedacusta

Historic vector
Incidental fauna
Introduction
Botanical gardens, first developed in the 1500s, have
been responsible for extensive movement of plants
for medicinal, crop, and ornamental purposes, and
more recently for education, scientific research and
ex situ conservation (Heywood 1987). Due to this
widespread dispersion, botanical and other public
gardens have been extremely important sites for the
introduction of non-indigenous plant species that
have subsequently established populations more
widely (Mack and Lonsdale 2001; Reichard and
White 2001). A commonly cited example is ‘‘Oxford
Ragwort’’ (Senecio squalidus), native to Sicily, which
invaded the United Kingdom (UK) from the Univer-
sity of Oxford Botanical Gardens (Mack 2005).
Gardens also have been responsible for the move-
ment of small animals as accidental hitchhikers on
plants. For example, the 1906 publication ‘‘The wild
fauna and flora of the Royal Botanic Gardens, Kew’’
provided a compilation of life recorded in Kew
Gardens that was not intentionally stocked there;
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examples included various insects, myriopods, spiders,
annelids, and even frogs, not native to the UK, which
had arrived there accidentally in association with plant
introductions (e.g., Beddard 1906; Günther 1906;
Pocock 1906). Similar incidental introductions have
included aquatic invertebrates. For example, the
freshwater jellyfish Craspedacusta sowerbii was first
recorded and described from the ‘Victoria regia’
(Victoria amazonica) tank at the Royal Botanic Soci-
ety’s Gardens in Regent’s Park, London (Lankester
1880), while the cladoceran Daphnia ambigua was
similarly first described from a pond in Kew Gardens,
London (Scourfield 1947). Craspedacusta is now
considered to be a native of China (Sowerby 1941),
while D. ambigua, now widespread in Europe, origi-
nated from the east coast of the United States (USA;
Hebert et al. 2003). Similarly, the Japanese calanoid
copepod species Sinodiaptomus valkanovi was first
described in 1938 from a population in the botanical
gardens in Sofia, Bulgaria (Ueda and Ohtsuka 1998),
was recorded again soon after in a lily pond in
California, USA (Light 1939), and more recently was
recorded in a greenhouse pond in New Zealand
(Duggan et al. 2006; Makino et al. 2010). The New
Zealand finding, along with the North American
Skistodiaptomus pallidus in another garden there
(Duggan et al. 2006), is recent, indicating the possibil-
ity of either continued movement of species by
gardens, or that there may be long-standing established
populations in garden ponds around the world, avail-
able to be spread more widely if provided opportunity.
Such ponds are apparently no longer common zoo-
plankton collection sites, so little is known of the
biodiversity inhabiting these ponds. In this study we
visited ten botanical and public gardens, three in the
UK and seven in the USA, to determine whether there
is a widespread presence of non-indigenous zooplank-
ton in garden ponds.
Methods
Forty man-made ponds from ten well-established
botanical and public gardens in the UK and USA
were sampled between 24 August 2010 and 28
September 2010 (Table 1). Four ponds were sampled
from most gardens, although three were sampled
at Oxford University Gardens (Oxford, UK) and
Lincoln Park (Chicago, USA), and five were sampled
123
I. C. Duggan, K. S. Duggan
at Kew Gardens (London, UK) and Missouri Botan-
ical Gardens (St. Louis, USA). Samples were col-
lected using a 2 l measuring jug, immersed into the
pond up to 0.5 m multiple times, with the water
passed through a 40 lm mesh. Volumes collected
ranged between 4 and 20 l (average 12.1 l), with the
final volume dependent on how easily the water
passed through the mesh. Material retained on the
mesh was preserved in ethanol ([50% final concen-
tration). Rotifers, cladocerans and copepods were
identified using various standard identification guides
(e.g., Lang 1948; Harding and Smith 1974; Koste
1978; Pennak 1978; Segers 1995).
Results
All ponds sampled were man-made. Twenty-one
ponds sampled were indoors, with the remaining
nineteen located outside (Table 1). Seventy-one roti-
fer, 19 cladoceran and 15 copepod (ten cyclopoid,
three calanoid, and two harpacticoid) taxa were
identified (Table 2). Rotifers were recorded in all
but one of the 40 ponds (97.5%), while copepods
(including nauplii) were found in 35 ponds (87.5%)
and cladocerans in 24 (60%). Species most frequently
encountered ([25%) were the littoral rotifers Lecane
hamata (21 of 40 ponds), L. closterocerca (20 ponds),
L. bulla (17 ponds), L. luna and Lepadella ovalis (11
ponds), and the cladoceran Chydorus sphaericus (11
ponds). Fifty species were recorded only once. None
of the species recorded represented non-indigenous
species in the areas sampled.
Discussion
We recorded no non-indigenous species during our
surveys, indicating that the threat of zooplankton
invasions from botanical garden ponds does not appear
to be great. This finding was surprising, given the rich
history of botanical gardens in spreading non-indige-
nous species, but may be indicative of two factors.
Firstly, many zooplankton populations that have estab-
lished in gardens are likely to have died out or had their
habitats destroyed in the intervening period. Secondly,
the probability of new non-indigenous species being
introduced to gardens from their native ranges by this
vector is now likely smaller than it was in the past.
Are botanical gardens a risk for zooplankton invasions? 2999

Table 1 Gardens and ponds sampled, showing location (I = inside, O = outside), code (#), sampling date, approximate date of
construction of ponds, and temperature at the time of sampling
Garden Pond/greenhouse L # Sample date Age 8C

Royal Botanic Gardens, Edinburgh, UK Rainforest Richess I 1 24 Aug 1967 23.4

Plants and people I 2 24 Aug 1967 26.5
Main Pond O 3 24 Aug Early 1800s 15.8
West Entrance O 4 24 Aug 2009 16.7
The University of Oxford Lily House I 5 01 Sep 1851 22.6
Botanic Garden, Oxford, UK Rock Garden O 6 01 Sep Early 1900s 16.5
Fountain O 7 01 Sep Early 1800s 15.1
Royal Botanic Gardens, Kew, London, UK Water Lily House I 8 03 Sep 1852 25.5
Temperate House I 9 03 Sep 1863 17.1
Main Lake O 10 03 Sep 1840s 18.1
Tropical Nursery I 11 03 Sep *1995 30.9
Princess of Wales I 12 03 Sep 1987 26.7
New York Botanical Gardens, New York City, NY, USA Haupt Conservatory O 13 16 Sep 1902 20.7
Conservatory, south I 14 16 Sep 1902 19.0
Rock Garden Pond O 15 16 Sep 1932 18.0
Propagation Tanks I 16 16 Sep Recent 22.9
Longwood Gardens, Kennett Square, PA, USA Hourglass Lake O 17 19 Sep 1965 19.9
Large Lake O 18 19 Sep 1700s 22.2
Conservatory O 19 19 Sep 1921 27.2
Chimes Tower Pond O 20 19 Sep 1931 20.5
Sarah P. Duke Gardens, Durham, NC, USA Main Pond O 21 21 Sep 1980 24.9
Blomquist Pond O 22 21 Sep 2008 22.8
Angle Pond O 23 21 Sep 2000 26.6
Peace Pond O 24 21 Sep 1994 23.2
United States Botanical Gardens, Washington DC, USA Regional Garden O 25 23 Sep 2001 25.5
Southern Exposure I 26 23 Sep 2001 25.1
Garden Primeval I 27 23 Sep 2001 24.4
Misting Jungle I 28 23 Sep 2001 24.8
Missouri Botanic Gardens, St. Louis, MO, USA Pond by Linnean O 29 26 Sep 1982 19.7
Pond by Climatron O 30 26 Sep 1917 20.0
Climatron/Nepenthes I 31 26 Sep 1989 21.3
Temperate House I 32 26 Sep 1989 22.0
Nursery Ponds I 33 26 Sep 2000 22.4
Lincoln Park Conservatory, Chicago, IL, USA Palm House I 34 28 Sep *1895 20.4
Show House, North I 35 28 Sep *1895 17.5
Show House, South I 36 28 Sep *1895 16.2
Garfield Park Conservatory, Chicago, IL, USA Lily Pool O 37 28 Sep 2005 17.8
Aroid House I 38 28 Sep 1907 18.8
Show Room I 39 28 Sep 1907 19.6
Fern Room I 40 28 Sep 1907 19.0

Populations of non-indigenous species may have of populations of the calanoid copepod Sinodiaptomus
been eliminated through destruction or cleaning of valkanovi from gardens in California and Bulgaria;
ponds. One well recorded example of this occurring is sampling of these populations was clearly fortuitous, as

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Table 2 Zooplankton recorded from garden pond samples

Rotifers
Anuraeopsis fissa—8, 18–19, 22 L. mira—22
Asplanchna girodi—21 L. pyriformis—17, 40
Brachionus angularis—17–18, 21, 29–30, 37 L. quadridentata—6, 17, 23
B. budapestinensis—13 L. stichaea—23
B. calyciflorus—30, 37 L. stokesi—15, 17
B. quadridentatus—13–15, 18, 23–24, 32–33 L. ungluata—17, 22
Cephalodella catellina—3 Lepadella accuminata—5, 31, 34, 36, 37
C. forficula—33 L. ovalis—3, 7, 15–17, 19, 25–27, 30, 38
C. gibba—14 L. patella—8, 14, 28
Cephalodella sp.—21 L. rhomboides—19
Colurella uncinata—1, 8, 19 Lindia torulosa—32
Collotheca sp.—17 Lophocharis oxysternon—37
Conochilus dossuarius—18 L. salpina—6, 17, 24
C. hippocrepis—21 Mytilina mucronata—7
Cupelopagis vorax—23, 34, 36–37 M. ventralis—11, 17, 36
Dicranophorus epicharis—1, 23, 37 Notommata cyrtopus—7
Euchlanis dilatata—17, 24, 26, 36 Plationus patulus—17
E. incisa—6, 21, 35 Proalinopsis squamipes—35
E. pyriformis—6 Polyarthra dolichoptera—6, 17–18
Eosphora thoides—24, 34–35 P. longiremis—10
Filinia novaezealandiae—18 P. vulgaris—29
Hexarthra mira—10 Proales daphnicola—15
Keratella americana—18, 21, 24 P. sigmoidea—8
K. cochlearis—6, 13, 18, 21, 37 Scaridium longicaudatum—6
K. cochlearis hispida—10 Synchaeta grandis—15
K. lenzi—24 S. oblonga—7–8
K. quadrata—7, 10, 12, 13 S. pectinata—18, 29, 33
K. tecta—37 Squatinella mutica—5, 8–9, 11, 15, 19, 22, 25, 36
Lecane bulla—1, 2, 8, 11, 14–19, 22–26, 34, 36 S. mutica tridentata—3, 5
L. closterocerca—1, 6–9, 15, 19, 22–23, 25–26, 28–32, 34, 36–38 Taphrocampa selenura—23
L. cornuta—17, 22 Testudinella patina—15
L. flexilis—1, 11, 13, 31–32, 37–38 Trichocerca multicrinis—21
L. hamata—1, 8, 11, 12, 14–17, 19, 22–24, 26, 28–29, 31–32, 34, T. similis—6, 13, 18, 21–22
36–38
L. hornemanni—8, 11, 16, 38, 40 T. vernalis—2, 7, 9, 19, 25–26, 34, 37
L. ludwigii luwigii—1 Bdelloids—1–3, 6, 8–12, 15–20, 22–30, 32–33, 35–39
L. luna—3, 17, 19–20, 22–23, 25–26, 32, 34–35
Cladocera
Alona affinis—21 Daphnia sp.—15
A. guttata—7, 17 Diaphanosoma brachyurum—21
A. rectangulata —12, 20, 30 Ilyocryptus agilis—2
Bosmina freyi—18 I. sordidus—15,18
B. liederi—13, 17, 21, 24 I. spinifer—37
B. longirostris—4 Pleuroxus aduncus—1, 4, 10
Ceriodaphnia quadrangula—10,17,21 P. denticulatus—6, 22, 35, 36

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Are botanical gardens a risk for zooplankton invasions?
Table 2 continued
C. reticulata—4, 24
Chydorus sphaericus—4, 7, 9, 10, 17, 18, 22, 25, 26, 35, 36
Daphnia galeata—7, 10
Copepods
Acanthocyclops brevispinosus—22
A. vernalis—4
Ectocyclops phaleratus—15, 25
Eudiaptomus gracilis—10
E. vulgaris—6
Epactophanes richardi—28, 35
Eucyclops serrulatus—15
Macrocyclops albidus—31
Mesocyclops leuckarti—6
Ostracods
Numbers refer to location codes (#) from Table 1
ponds responsible for both of these records have
subsequently been destroyed (Ueda and Ohtsuka
1998). Similar destruction and re-creation of ponds
within gardens is apparently common, such as during
refurbishment and restoration of greenhouses. The Lily
House at the University of Oxford Botanic Gardens,
and the Enid A. Haupt Conservatory at New York
Botanical Gardens, for example, have each been
refurbished and reconstructed on several occasions
since their openings in 1851 and 1902, respectively
(Soderstrom 2001; Mayou and Matthews 2010). Dur-
ing our surveys, the Enid A. Haupt Conservatory was
again closed for refurbishment, as was the Linnean
House at Missouri Botanical Gardens, and at the Sarah
P. Duke Gardens an entire outdoor pond had been
drained and was in the process of reconstruction. Even
the relatively new Climatron at the Missouri Botanical
Gardens, built in 1960, had extensive renovations
undertaken between 1988 and 1990, which involved
re-landscaping almost the entire interior (M. Gray,
Mobot, pers. comm.; www.mobot.org). Ponds are also
occasionally emptied and cleaned, and therefore the
number of non-indigenous populations in gardens,
such as those of S. valkanovi, may steadily decrease
through time. The presence of small zooplanktivorous-
sized fish was commonly observed in conservatory
ponds. When this became common practice is unclear,
although such fish are likely to exert strong predation
pressure on crustacean zooplankton (Brooks and
3001
Scapholeberis mucronata—22, 35–37
Simocephalus vetulus—22, 26, 29, 30, 33, 35, 36
Microcyclops rubellus—21, 22, 26, 27, 31
M. varicans—33, 35
Paracyclops chiltoni—20, 28, 36
Phyllognathopus vigueri—27, 32, 39, 40
Skistodiaptomus pallidus—21
Tropocyclops prasinus—7, 17, 25, 31
indet cyclopoids—1, 2, 10, 14, 18, 24, 32, 39
nauplii—1–8, 10–15, 17–22, 24–31, 33, 35–37, 40
4, 5, 7, 8, 10, 11, 15, 17, 18, 21, 22, 24–27, 29–31, 33, 35–37,
39
Dodson 1965). Finally, insecticides used to protect
plants, if these enter the ponds, may also be responsible
for the destruction of crustacean populations (e.g.,
Onbasili and Duman 2010).
While populations of non-indigenous species are
seemingly being extirpated from gardens, they are
likely not being replaced at a commensurate rate.
Conservation and science are increasing in impor-
tance, with many gardens beginning to place a greater
focus on native plants, resulting in a decline in the
value of aesthetics and the display of plants of
interesting or unusual morphology (Soderstrom 2001;
Pennisi 2010). As such, the introduction to botanical
gardens of new plants from foreign countries is not
generally a major concern (Heywood 2011). Codes of
conduct have also been introduced by botanical
gardens that tighten the restrictions on movement
and sale, particularly for plants that may spread or
become harmful (Baskin 2002; Reichard 2004). As
such, new aquatic plants are likely not entering
botanical gardens from the wild, and their display has
declined in importance. Many gardens do, however,
still display Victoria lilies, although these will now be
sourced from other gardens rather than being wild
collected (the most commonly displayed variety
being the Longwood hybrid). However, although
reduced in importance, this is not to say that new
plants do not still enter some botanic gardens from
wild caught collections (Heywood 2011).
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3002
Although we found no evidence of non-indigenous
species in our surveys, there have been other recent
examples of small aquatic non-indigenous inverte-
brates recorded from ponds in public gardens (e.g.,
the copepods Mesocyclops pehpeiensis and Arctodia-
ptomus dorsalis in Kenilworth Aquatic Gardens,
Washington DC, USA; Reid 2008). Additionally,
while we sampled ponds, a number of studies have
recorded copepods from water pools in bromeliads
(Reid 2001; Reid and Hribar 2006) and from the soil
of plant nurseries (Reid 1999; Bruno et al. 2005).
This infers that some gardens do possess non-
indigenous species available for spread, and that
there are other means by which small aquatic animals
may be transported in association with plants among
public gardens. However, the prevalence of such
invaders in New Zealand garden ponds is seemingly
an anomaly relative to the gardens visited in current
study. Indeed, the North American calanoid copepod
Skistodiaptomus pallidus was first recorded in New
Zealand from the Auckland Botanical Gardens, a
relatively new garden opened in 1982, but has also
been recorded as a contaminant among Daphnia sold
as live food for aquarium fish (Duggan et al. 2006).
This, along with it subsequently having been found in
other New Zealand ponds not associated with gardens
(Banks and Duggan 2009), indicates an introduction
vector other than gardens. On the whole, however,
movement of plants among garden ponds is likely not
common, in contrast to the aquarium trade where
plants are still constantly being dispersed, moving
small invertebrate species with them (Duggan 2010).
With aquarium fish currently being used in many
conservatory ponds, new non-indigenous zooplank-
ton species may now have a greater probability of
entering garden ponds via this vector than in asso-
ciation with garden plants.
Overall, we found no evidence that public gardens,
or at least gardens in the UK and USA that are well
established, provide a high risk of introduction of
new aquatic animals. However, it must be acknowl-
edged that although we sampled well established,
‘iconic’ gardens, these represent only a small pro-
portion of the botanic gardens of the world. Gardens
that continue to introduce new plants in modern times
perhaps still provide a risk of spreading non-indig-
enous zooplankton as fellow travellers, except where
international, organisational or other policies are in
place to reduce the movement of incidental species to
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I. C. Duggan, K. S. Duggan
those gardens. We recommend the surveying of
garden ponds in other regions, and of other aquatic
habitats in gardens, to more fully elucidate the
importance of this vector.
Acknowledgments We thank all those gardens that agreed to
allow us to take samples from their ponds, and those employees
that took their time to guide us and provide information on the
ponds; P. Brownless (RBGE), P. Morris (Kew), K. Pritchard
(Oxford), J. Arcate Schuler (NYBG), R. Mottern III (Duke),
C. Flanagan (USBG), M. Gray (Mobot), C. Sclar (Longwood)
and M. Eysenbach (Chicago Parks). We thank R. Keller
(U. Chicago) and M. Williamson (U. York) for providing
preservative. J. Muirhead (Smithsonian Institute), J. Banks
(Waikato) and H. Hodges aided in shipping samples.
H. MacIsaac, J. Reid and an anonymous reviewer provided
comments that improved our manuscript.
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