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The Partnership between Gobiid Fishes and Burrowing Alpheid Shrimps

Abstract and Figures

The association between non-burrowing gobiid fishes and burrowing alpheid shrimps is a mutualistic, co-evolved partnership. The shrimp constructs and maintains a burrow which is used by the goby as a temporary shelter during the day, a permanent resting place over night and a safe place for breeding. The goby provides the shrimp with a tactile based alarm system, warning it against approaching predators or fish that dig in the sediment and may block its burrow entrance. A detailed review of the information available on goby-shrimp associations was published twenty years ago (Karplus, 1987). The aim of the present review is to focus mainly on new findings that cover a wide range of topics including goby-shrimp taxonomy, biogeography, ecology, behavior, partner specificity, phylogeography and evolution. However, in order to expose the reader to the full picture of these fascinating associations, older studies will be briefly reviewed at the beginning of each section. In some areas of research (e.g. goby and shrimp reproduction) few or no studies were carried out over the last twenty years. In these cases a more detailed overview based on older studies will be presented.
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CHAPTER
The Partnership between
Gobiid Fishes and Burrowing
Alpheid Shrimps
Ilan Karplus
1
and Andrew Richard Thompson
2
4.4
INTRODUCTION
e association between non-burrowing gobiid  shes and burrowing alpheid
shrimps is a mutualistic, co-evolved partnership.  e shrimp constructs
and maintains a burrow which is used by the goby as a temporary shelter
during the day, a permanent resting place over night and a safe place for
breeding.  e goby provides the shrimp with a tactile based alarm system,
warning it against approaching predators or  sh that dig in the sediment
and may block its burrow entrance. A detailed review of the information
available on goby-shrimp associations was published twenty years ago
(Karplus, 1987).  e aim of the present review is to focus mainly on new
ndings that cover a wide range of topics including goby-shrimp taxonomy,
Authors’ addresses:
1
Aquaculture Research Unit, the Institute of Animal Sciences,  e Volcani
Research Center, P.O. Box 6, Bet-Dagan 20250, Israel. E-mail: karplus@agri.gov.il
2
NOAA Fisheries Service, Southwest Fisheries Science Center, 8604 La Jolla Shores Drive, La
Jolla, CA 92037-1508, USA. E-mail: andrew.thompson@noaa.gov
560 e Biology of Gobies
biogeography, ecology, behavior, partner speci city, phylogeography and
evolution. However, in order to expose the reader to the full picture of
these fascinating associations, older studies will be brie y reviewed at the
beginning of each section. In some areas of research (e.g. goby and shrimp
reproduction) few or no studies were carried out over the last twenty years.
In these cases a more detailed overview based on older studies will be
presented.
SYSTEMATICS OF GOBIES AND SHRIMPS
The majority of studies addressing the goby-shrimp partnership focus
mostly on the description of new gobies without describing their behavior,
ecology or interrelationship with their shrimp partners. Historically,
description of associated gobies lagged behind the description of other
coral reef  shes, due to the habit of the gobies to shelter inside the shrimp-
constructed burrow when disturbed.  ese species were o en not collected
with traditional collecting techniques such as large scale indiscriminate
poisoning.  e advent of SCUBA diving and selective  sh collecting using a
variety of techniques reviewed in Karplus (1987) resulted in the continuous
discovery of many species of associated gobies, particularly in the tropical
Indo-Paci c.
Close to forty new species of gobies associated with shrimps were
described over the last twenty years (Table 4.4.1). Over 120 species of
associated gobies belonging to more than twenty di erent genera are now
known to live in association with burrowing alpheid shrimps (Karplus,
1987; Table 4.4.1). Previous and current debates concerning the generic
a nity of associated gobies (e.g. Ikeda et al.. 1995; Chen and Fang, 2003;
Shibukawa and Suzuki, 2004; Iwata et al., 2007; Randall, 2007b; Randall
and Chen, 2007), contributed to the common occurrence of synonymy.
roughout this text we adopted the taxonomic classi cation presented at
the FishBase website (Froese and Pauly, 2008).
Although the nature of the relationship between gobies and shrimps is
not known for some species, many species of gobies interact either obligately
or facultatively with shrimps.  e obligate species belong to twelve genera
that consist exclusively of gobies that associate with shrimps (but see below
for a possible exception). The two most speciose genera are the Indo-
Paci c genera Amblyeleotris and Cryptocentrus, each containing over thirty
described species. Amblyeleotris species share a pair of sensory papillae
at the center of the lower lip, and the presence of both transverse and
Ilan Karplus and Andrew Richard  ompson 561
Table 4.4.1 New species of gobies associated with shrimps (and reported depth
distribution) described over the last 20 years (1987-2007).
Fish Species Distribution and Depth Shrimp Partner References
Amblyeleotris Papua New Guinea Alpheus bellulus Mohlmann and
arcupinna (23 m) Munday, 1999
Amblyeleotris New Caledonia not described Randall, 2004
bellicauda Papua New Guinea
(3 m)
Amblyeleotris Solomon Islands not described Randall, 2004
biguttata New Caledonia
(11-50 m)
Amblyeleotris Arabian Gulf Alpheus bellulus Randall, 1994
downingi (13-17 m) Alpheus
ochrostriatus
Amblyeleotris New Caledonia not described Randall, 2004
ellipse Papua New Guinea
Amblyeleotris Christmas Island not described Mohlmann and
harrisorum (32 m) Randall, 2002
Amblyeleotris Mariana and Marshall Alpheus Randall, 2004
katherine Islands, American Samoa ochrostriatus
Cook and Society Islands
(3-38 m)
Amblyeleotris Marquesas Islands Alpheus randalli Mohlmann and
(20-25 m) Randall, 2002
Amblyeleotris Okinoshima and Okinawa not described Aonuma et al.,
melanocephala Islands, Japan 2000
Amblyeleotris Ryukyu Islands, Japan not described Aonuma and
nasuii (35-40 m) Yoshino, 1996
Amblyeleotris New Britain Alpheus rapacida Randall and Earle,
neumanni Papua New Guinea and additional non 2006
(26 m) described species Mohlmann and
Amblyeleotris Great Barrier Reef not described Randall, 2002
rubrimarginata New Caledonia,
(3-26 m)
Amblyeleotris New Caledonia Alpheus bellulus Randall, 2004
stentaeniata (10-20 m)
Amblyeleotris Red Sea, Gulf of Oman Alpheus bellulus Randall, 1994
triguttata Arabian Gulf
(1.5-17 m)
Ambleyleotris Ryukyu Islands, Japan Alpheus randalli Aonuma and
yanoi (3-30 m) Yoshino, 1996
Ctenogobiops Taiwan not described Randall et al.,
formosa 2003
Contd...
562 e Biology of Gobies
Contd...
Fish Species Distribution and Depth Shrimp Partner References
Ctenogobiops South China Sea, Marshall not described Randall et al.,
mitodes Islands, Solomon Islands, 2007
Papua New-Guinea
(2-21m)
Ctenogobiops Papua New-Guinea expected to be Randall et al.,
phaeostictus (10 m) associated with a 2007
shrimp
Flabelligobius Taiwan expected to be Chen and Fang,
smithi (100 m) associated with a 2003
shrimp
Stonogobiops Kochi prefecture, Japan Alpheus randalli Iwata and Hirata,
pentafasciata (18-40 m) Alpheus bellulus 1994
Stonogobiops Ryukyu Islands, Japan Alpheus randalli Yoshino and
yasha Palau Islands Shimada, 2001
New Caledonia and
Bali, Indonesia
(15-40 m)
Tomiyamichthys Japan and Indonesia not described Iwata et al. 2000
alleni
Tomiyamichthys Island of Flores, Indonesia Alpheus cf. Randall and Chen,
tanyspilus (4 m) rapacida 2007
Vanderhorstia Solomon Islands expected to be Randall, 2007b
attenuata (38-48 m) associated with a
shrimp
Vanderhorstia Molluca Islands, Indonesia expected to be Randall, 2007b
auronotata associated with a
shrimp
Vanderhorstia Fiji Islands not described Green eld and
bella (8 m) Longenecker, 2005
Vanderhorstia Papua New Guinea expected to be Randall, 2007b
belloides (21m) associated with a
shrimp
Vandrhorstia Papua New Guinea Alpheus rapacida Randall, 2007b
dorsomacula (25m)
Vanderhorstia Papua New Guinea not described Allen and
avilineata (15-30 m) Munday, 1995
Vanderhorstia Japan, not described Iwata et al., 2007
hiramatsui (30m)
Vanderhorstia Japan not described Iwata et al., 2007
kizakura (45m)
Vanderhorstia* Indonesia Expected to be Weber, 1909
longimanus (118 m) associated with a Iwata
et al., 2007
shrimp
Contd...
Ilan Karplus and Andrew Richard  ompson 563
Fish Species Distribution and Depth Shrimp Partner References
Vanderhorstia* Japan not described Franz, 1910
macropteryx (20-110 m) Ikeda et al., 1995
Vanderhorstia Palau and Philippines not described Winterbottom
nannai (0-15 m) et al., 2005
Vanderhorstia Philippines, Sulawesi, not described Allen and Randall,
nobilis Indonesia (5-25 m) 2006
Vanderhorsta Red Sea Alpheus bellulus Randall, 2007a
opercularis (27-40m) Alpheus
ochrostriatus
Vanderhorstia Ryuku Islands, Japan not described Shibukawa and
papilio (45 m) Suzuki, 2004
Vanderhorstia Japan (60-123) expected to be Deng and Xiong,
puncticeps China (76-98) associated with a 1980
shrimp Iwata et al., 2007
Vanderhorstia Japan not described Deng and Xiong,
rapa (25-50 m) 1980; Iwata et al.,
2007
* not described before associated with shrimp
Contd...
longitudinal cheek papillae rows (Hoese and Steene, 1978; Winterbottom,
2002).  e genus Cryptocentrus also has both transverse and longitudinal
papillae rows, but differs from Amblyeleotris in having fewer dorsal fin
rays, cycloid scales only (rather than ctenoid), and di erences in papillae
pattern and head shape (Chen et al., 1998; Mohlman and Randall, 2002).
The genera Vanderhorstia and Ctenogobiops consist of an intermediate
number of species. Ctenogobiops was recently reviewed by Randall et al.
(2003) and  acker et al. (2010); it shares with Vanderhorstia characters of
n ray counts, scalation, head and tongue shape, and sensory pore pattern.
e two genera are distinguished only by caudal  n length: longer and
more tapered in Vanderhorstia as compared to Ctenogobiops (Shibukawa
and Suzuki, 2004). Genera such as the Atlantic Nes and the Indo-Paci c
Lotilia contain only one described, associated species. Additional genera
that contain obligatory shrimp gobies are Psilogobius, Flabelligobius,
Tomiyamichthys, Myersina and Mahidolia.
At present there are only  ve reports of facultative associations between
gobies and burrowing alpheid shrimps. Bathygobius curacao (Karplus, 1992)
and Ctenogobius saepepallens (Randall et al., 2005 ; Kramer et al. 2009)
were both reported in a facultative partnership with Alpheus  oridanus
from the Western Atlantic. Three additional facultative fish partners
were reported from the Indo-Paci c: Vireosa hanae (Yanagisawa, 1978),
Acentrogobius p aumi (Yanagisawa, 1978) and Cryptocentrus singapurensis
564 e Biology of Gobies
(Palomar, 2001). Facultative gobies apparently belong to genera that
include only a single or few associated species and a large number of free
living gobies. For example, the facultative Atlantic Bathygobius curacao
(Karplus, 1992), is the only associated goby in a genus which contains
36 free living species. Similarly, the facultative Indo-Paci c Acentrogobius
p aumi (Yanagisawa, 1978), is the only associated goby in a large genus that
contains an additional 21 free living species. However, the facultative  sh
partner Cryptocentrus singapurensis belongs to a genus previously known to
contain only obligatory  sh partners.
At present there has not been a comprehensive analysis of the evolutionary
relationship among the di erent genera and species of obligatory, facultative
and free living species (but see evolution section of this review). Such an
analysis based on morphological traits and molecular markers could be
very important for the understanding of the evolution of the goby-shrimp
partnership.
Our understanding of the taxonomy of goby-associated alpheid shrimps
was poor twenty years ago (Karplus, 1987), and remains confused and
incomplete to this day. Currently, there are fourteen described species
(Alpheus bellulus, A. bisincisus, A. brevicristatus, A. brevirostris, A. djeddensis,
A. djiboutensis, A. fenneri, A.  oridanus, A. crassimanus, A. macellarius, A.
malabaricus, A. randalli, A. rapacida and A. rapax Karplus, 1987; Talwar
and Jhingram, 1991; Table 4.4.2).  ere are three additional species (A.
purpurilenticularis, A. ochrostriatus and A. rubromaculatus) that have not
been formally described but their names were given to Karplus by Miya
a er a detailed morphological study. Photos of the latter three species and
their color description were presented by Karplus et al. (1981).  ese three
associated shrimps were  rst described from the Red-Sea and later reported
in several popular and scienti c publications (Debelius, 1999; Randall, 1994,
2004) from di erent localities in the Indo-Paci c. ere is urgent need for
the formal description of these three species as their current names are
invalid without proper description. In addition to the described and semi-
described alpheid species, numerous shrimp “types” were noted by several
researchers.  ese types were di erentiated by distinct colorations in studies
carried out in the Seychelles (Polunin and Lubbock, 1977; 7 types), the
Great Barrier Reef (Cummins, 1979; 4 types), Palau (Sakaue et al., 2005;
3 types) and  ailand (Nakasone and Manthachitra, 1986; 1 type).
Elucidating alpheid shrimp taxonomy is made difficult by two main
factors. First, goby-associated shrimps are difficult to collect even in
comparison with their goby partners. Whereas gobies sometimes wander
away from a burrow, shrimp always retreat into the burrow when disturbed
Ilan Karplus and Andrew Richard  ompson 565
and are virtually impossible to excavate. Although techniques have been
developed to catch these elusive shrimps (Karplus and Vercheson, 1978;
Karplus, 1987), collection is still a time-intensive process. Second, alpheid
shrimps are known to exhibit a high degree of cryptic speciation (Knowlton,
1993;  ompson et al., 2005; Matthews, 2006) and are morphologically
variable within a species. To clarify species distinctions it is necessary to
not rely solely on museum work with dead specimens but to also make
careful  eld observations (such as live coloration, goby partner identity
and preferred microhabitat) and conduct laboratory studies on live
specimens (Banner and Banner, 1982; Anker, 2000).  ere is a real need
for the description of associated alpheid shrimp species and analysis of
their relatedness and relationship with free living species.  is analysis can
be achieved by combining classical morphological,  eld observations and
molecular techniques.
BIOGEOGRAPHY
Over the past two decades several studies have helped to further our
understanding of how patterns of goby and shrimp species richness vary
around the world. For example, Randall et al. (2005, 2007) examined
the distribution and described three new species of gobies in the genus
Ctenogobiops. Recent reviews and species descriptions of the genera
Amblyeleotris (Aonuma and Yoshino, 1996; Chen et al., 1998; Mohlmann and
Randall, 2002; Denou and Aonuma, 2007), Cryptocentrus (Winterbottom,
2002; Koichi et al., 2005), Flabelligobius (Chen and Fang, 2003; Koichi
et al., 2005), Myersina (Winterbottom, 2002), Stonogobiops (Winterbottom,
2002), Tomiyamichthys (Iwata et al., 2000; Randall and Chen, 2007) and
Table 4.4.2 New species of shrimps associated with gobies described during the last 20
years (1987-2007)* and earlier described species of shrimps not reported before as living
with gobies**.
Shrimp species Distribution and Depth Fish partner References
Alpheus djeddensis** South Paci c Ctenogobiops ompson, 2005
feroculus
Alpheus fenneri* Sulawesi, Indonesia Amblyeleotris Bruce, 1994
(6 m) fontannesii
Alpheus macellarius* Philippines Cryptocentrus Palomar et al., 2004,
octafasciatus, 2005
Cryptocentrus Chace, 1988
singapurensis
566 e Biology of Gobies
Vanderhorstia (Randall, 2007) have also expanded our knowledge of the
distribution of Indo-Paci c associated gobies. Although the rate at which
new species of associated gobies are being discovered indicates that there
is still much work to be done to fully elucidate global patterns of species
richness of associated gobies and shrimps, much progress has been made in
this direction since this association was reviewed by Karplus (1987).
Despite the recent research on the distribution of di erent goby genera,
at present there has not been a synthetic, quantitative examination of the
relationship between latitude and longitude on variability in species richness
of associated gobies and shrimps. To evaluate how species richness changes
with global location, we compiled species lists from several locations in the
Indo-Paci c. Our primary source for site-speci c sh species information
was the FishBase website (Froese and Pauly, 2008), but we also reviewed
species accounts from the recent literature (e.g. Randall, 2007; Randall and
Chen, 2007). Because species lists are not necessarily comprehensive in
the Fish Base database, we restricted our analysis to locations that met at
least one of the following conditions: 1) speci c studies on shrimp gobies
had been conducted at the location (Red Sea, Seychelles, Maldives), 2)
comprehensive surveys of  sh diversity were made at the location (Red
Sea, Taiwan, Guam, Indonesia, Papua New Guinea), and/or 3) we had
personally collected associated gobies and shrimps at the location (Red Sea,
Society Islands, Fiji, Papua New Guinea, Taiwan). If we identi ed associated
gobies that were not included in the  shbase.org database for a particular
site, we added them to the list. It is important to note that the species lists
generated for this analysis incorporate those species that are con rmed as
being present at a location and that absence of a species does not necessarily
indicate that it is not present at a given locality. We restricted our analysis
to include only species of gobies that depend obligately on shrimps.
We tested the hypothesis that goby and shrimp diversity is maximal near
Indonesia and decreases away from this location (Bellwood and Hughes
2001). Despite the caveats associated with our data, results reveal a clear
pattern: species richness of associated gobies peaks near Indonesia and
decreases away from this center of diversity (Figure 1-A, Table 4.4.3A).
Indeed, we identi ed 46 species of associated gobies that are recorded in
Indonesia (Table 4.4.1A). By contrast, islands west of Indonesia are reported
to contain 16 (Maldives) and 13 species (Seychelles). Taiwan, which is
approximately 3000 kilometers north of Indonesia contains a reported 22
associated species. Diversity also drops as distance increases eastward from
Indonesia as records indicate that Papua New Guinea contains 36 species,
Ilan Karplus and Andrew Richard  ompson 567
Table 4.4.3 A. Species of gobies that are obligately associated with alpheid shrimps from several locations in the Indo-Paci c. Species were
primarily identi ed using Froese and Pauly (2008). Superscript numbers indicate species that were identi ed by the following sources:
1
Mous
et al., 2005;
2
photographed and/or collected and deposited in the Section of Fishes of the Natural History Museum of Los Angeles County by
Andrew  ompson;
3
Allen and Munday, 1999, Checklist of the Fishes of Kimbe Bay, Papua New Guinea (www.walindi.com/ sh),
7
Randall, 2007,
8
Iwata et al., 2000,
9
Randall and Chen, 2007,
10
Randall et al., 2007. B. Species of shrimps which are obligately associated with gobies from several
locations in the Indo-Paci c. All sites were visited by Andrew  ompson and/or Ilan Karplus except Hawaii. Superscript numbers indicate
the source of shrimp species information:
2
same as above;
4
same shrimp as identi ed by Masayoshi and Shiratori, 2003;
5
Karplus et al., 1981,
6
unknown shrimp,
11
Preston, 1978 and Nelson, 2005.
Indonesia Papua New Guinea Taiwan Maldives Seychelles Red Sea Fiji Society Islands Hawaii
Amblyeleotris arcupinna
1
Amblyeleotris arcupinna
3
Amblyeleotris fasciata Amblyeleotris aurora Amblyeleotris aurora Amblyeleotris diagonalis Amblyeleotris guttata
2
Amblyeleotris katherine
2
Psilogobius mainlandi
Amblyeleotris aurora Amblyeleotris diagonalis Amblyeleotris fontanesii Amblyeleotris diagonalis Amblyeleotris diagonalis Amblyeleotris fasciatus Amblyeleotris periophthalma
2
Ctenogobiops fercoculus
2
Amblyeleotris diagonalis Amblyeleotris fontanesii Amblyeleotris guttata Amblyeleotris periophthalma Amblyeleotris periophthalma Amblyeleotris steinitzi Amblyeleotris steinitzi
2
Mahidolia mystacina
Amblyeleotris fasciata Amblyeleotris guttata Amblyeleotris periophthalma Amblyeleotris steinitzi Amblyeleotris sungami Amblyeleotris sungami Amblyeleotris randalli Vanderhorstia ornatissima
Amblyeleotris fontanesii Amblyeleotris gymnocephala Amblyeleotris steinitzi Amblyeleotris wheeleri Cryptocentrus cryptocentrus Amblyeleotris triguttata Amblyeleotris wheeleri
Amblyeleotris guttata Amblyeleotris novaecaledoniae Amblyeleotris wheeleri Cryptocentrus fasciatus Cryptocentrus fasciatus Amblyeleotris wheeleri Ctenogobiops aurocingulus
Amblyeleotris gymnocephala Amblyeleotris periophthalma Cryptocentrus albidorsus Cryptocentrus strigilliceps Ctenogobiops crocineus Cryptocentrus caeruleopunctatus Ctenogobiops crocineus
2
Amblyeleotris periophthalma Amblyeleotris randalli Cryptocentrus cryptocentrus Ctenogobiops crocineus Ctenogobiops feroculus Cryptocentrus cryptocentrus Ctenogobiops ferocululs
2
Amblyeleotris latifasciata
1
Amblyeleotris rhyax Cryptocentrus nigrocellatus Ctenogobiops feroculus Stonogobiops dracula Cryptocentrus fasciatus Ctenogobiops mitodes
10
Amblyeleotris randalli Amblyeleotris steinitzi Cryptocentrus strigilliceps Flabelligobius latruncularia Stonogobiops nematodes Cryptocentrus lutheri Ctenogobiops pomastictus
2
Amblyeleotris steinitzi Amblyeleotris wheeleri Ctenogobiops aurocingulus Stonogobiops dracula Vanderhorstia delagoae Ctenogobiops crocineus Cryptocentrus koumansi
Amblyeleotris wheeleri Amblyeleotris yanoi Ctenogobiops crocineus
Tomiyamichthys latruncularius
9
Vanderhorstia ornatissima Ctenogobiops feroculus
Cryptocentrus strigilliceps
2
Amblyeleotris yanoi Cryptocentrus cinctus Ctenogobiops feroculus Tomiyamichthys praealta
9
Vanderhorstia praealta Flabelligobius latruncularia Lotilia graciliosa
Cryptocentrus albidorsus Cryptocentrus cyanotaenia Ctenogobiops formosa Vanderhorstia ambanoro Tomiyamichthys fourmanoiri
9
Vanderhorstia bella
Cryptocentrus caeruleomaculatus Cryptocentrus fasciatus Ctenogobiops pomastictus Vanderhorstia ornatissima Vanderhorstria delagoae
Cryptocentrus cinctus Cryptocentrus inexplicatus
2
Ctenogobiops tangaroai Vanderhorstia praealta Vanderhorstia mertensi
Cryptocentrus cyanotaenia Cryptocentrus leptocephalus Flabelligobius smithi Vanderhorstria opercularis
7
Cryptocentrus fasciatus Cryptocentrus leucostictus Lotilia graciliosa
Cryptocentrus inexplicatus Cryptocentrus octofasciatus
3
Mahidolia mystacina
Cryptocentrus leptocephalus Cryptocentrus singapurensis Myersina yangii
Cryptocentrus leucostictus Cryptocentrus strigilliceps Tomiyamichthys smithi
9
Cryptocentrus maudae Cryptocentrus sp. A Vanderhorstia mertensi
Cryptocentrus nigrocellatus Ctenogobiops aurocingulus
Cryptocentrus octofasciatus
1
Ctenogobiops crocineus
Cryptocentrus strigilliceps Ctenogobiops feroculus
Cryptocentrus sp. 2
1
Ctenogobiops mitodes
10
Cryptocentrus sp. 3
1
Ctenogobiops phaeostictus
10
Cryptocentrus sp. 4
1
Ctenogobiops pomastictus
Ctenogobiops aurocingulus Ctenogobiops tangaroai
Ctenogobiops crocineus Lotilia graciliosa
Ctenogobiops feroculus Mahidolia mystacina
Ctenogobiops mitodes
10
Myersina lachneri
3
Ctenogobiops pomastictus Stonogobiops xanthorhinica
Ctenogobiops tangaroai Tomiyamichthys oni
Ctenogobiops sp.
2
Vanderhorstia ambanoro
Lotilia graciliosa Vanderhorstia lanceolata
Mahidolia mystacina Vanderhorstia mertensi
Myersina nigrivirgata
1
Vanderhorstia ornatissima
Myersina filifer
Myersina papuanus
Stonogobiops nematodes
Stonogobiops xanthorhinica
Tomiyamichthys alleni
8
Tomiyamichthys oni
Tomiyamichthys tanyspilus
9
Vanderhorstia ambanoro
Vanderhorstia lanceolata
A
568 e Biology of Gobies
Papua New Guinea
Taiwan
Red Sea
Fiji
Society Islands
Alpheus bellulus
2
Alpheus bellulus
2
Alpheus bellulus
5
Alpheus djeddensis
2
Alpheus djeddensis
2
Alpheus brevicristatus
2
Alpheus djeddensis
2
Alpheus djiboutensis
5
Alpheus ochrostriatus
2
Alpheus ochrostriatus
2
Alpheus djeddensis
2
Alpheus djiboutensis
2
Alpheus ochrostriatus
5
Alpheus rapax
2
Alpheus rapax
2
Alpheus ochrostriatus
2
Alpheus ochrostriatus
2
Alpheus rapax
5
Alpheus sp. 5 pink
2
Alpheus randalli
2
Alpheus rubromaculatus
2
Alpheus rubromaculatus
5
Alpheus rapax
2
Alpheus
sp.
5, 6
Alpheus sp. 1
2,4
Alpheus sp. 5 pink
2,4
Alpheus sp. 7 white
2,4
Alpheus sp. A
2,6
Alpheus rapicida
11
Alpheus rapax
11
Hawaii
B
Ilan Karplus and Andrew Richard  ompson 569
Fig. 4.4.1 Species richness of associated gobies and shrimps in the Indo-Paci c. A.
Minimum number of obligately associated shrimp-goby species from ten locations in the
Indo-Paci c. B. Minimum number of shrimp species that are obligately associated with
gobies from six locations in the Indo-Paci c.
570 e Biology of Gobies
Guam 15 species, Fiji 13 species, and French Polynesia four species.  e
most distant site, Hawaii, harbors only one species of associated goby.
Patterns of species richness appear to be similar for obligately associated
shrimps. Because there are few published, comprehensive site-specific
surveys for alpheid shrimps in the Indo-Paci c, we present unpublished
data from our own research on Papua New Guinea, Taiwan, Fiji, and the
Society Islands ( ompson and  acker, unpublished data) and published
reports from the Red Sea (summarized in Karplus 1987). In addition, we
include information on shrimp species from Hawaii where the list is likely
complete. We collected and/or surveyed ten associated shrimps in Papua
New Guinea, three in Taiwan, three in Fiji, and three in French Polynesia.
In Hawaii, two species of associated shrimps are reported (Nelson, 2005).
While these surveys were not necessarily comprehensive across all habitat
types in these locations, the pattern of decreasing diversity away from
Indonesia is similar to that shown by associated gobies (Fig. 4.4.1B, Table
4.4.3B). As mentioned in the Systematics section of this review, better
elucidation of shrimp taxonomy may further clarify how species richness
varies across coral reefs worldwide.
Our nding that goby and shrimp diversity peaks near Indonesia and
declines eastward and westward parallels studies of other coral reef taxa
(Bellwood et al., 2005). A number of hypothesis exist to explain the notably
high species diversity of marine organisms in the Indo-West Paci c (IWP)
(reviewed in Palumbi, 1996, 1997).  e center of origin model postulates
that species arose in the IWP region in the west, and dispersed eastward.
The center of accumulation model holds that speciation took place in
outlying archipelagos such as Hawaii, the Marquesas Islands or the
Society Islands, followed by dispersal westward into the IWP.  e center
of overlap model would indicate no consistent pattern for speciation or
dispersal, because IWP diversity would simply be an artifact of overlapping
biogeographic provinces in which speciation and dispersal occurred
throughout. Although it is di cult to de nitively state that one or more
of these hypothesis explains the gradient in associated goby and shrimp
species richness,  ompson et al. (2005) showed that decreasing within-
site genetic diversity for Ctenogobiops feroculus and Alpheus djeddensis in
an eastward direction is consistent with dispersal away from the center of
diversity (see goby-shrimp phylogeography chapter in this review). Further
molecular work on more goby-shrimp taxa could further elucidate causal
patterns of the biogeographic gradient in the species richness of associated
gobies and shrimps.
Ilan Karplus and Andrew Richard  ompson 571
Whereas most of the research on goby-shrimp partnerships focused on
obligate, Indo-Paci c genera, associated gobies and shrimps are also found
in the Atlantic. Five species of gobies (Bathygobius curacao, Gobionellus
saepepallens, Gobionellus stigmalophius, and Nes longus) are known to
associate with burrowing alpheid shrimp in the western Atlantic. Of these
species only Nes longus maintains an obligate relationship with its shrimp
partner (Karplus, 1992; Randall et al., 2005; Kramer et al. 2009).  us it
appears that although the total number of goby species that associate with
shrimp is much lower in the Atlantic than the Indo-Paci c, the proportion
of species that interact facultatively with shrimp may be higher in the
Atlantic. Additional research on the relative number of facultative and
obligate species in di erent parts of the world is needed to con rm this
pattern.
ECOLOGY
Demographic Impacts of the Mutual Partnership
Although it is well established that many species of gobies and alpheid
shrimps may participate in this mutualism, the exact nature of the bene ts
provided by each partner are not fully understood. From a demographic
perspective, the mutual bene ts are re ected through either an augmentation
in rates of birth or a reduction in rates of death ( ompson et al., 2006).
Given the abundance of predators on coral reefs, it is generally believed that
the primary function of the goby-shrimp mutualism is to directly reduce
the rates of death for both partners (Karplus, 1987; Nelson, 2005). From the
perspective of the goby, the shrimp provides a burrow within which the  sh
seeks shelter from predators, thus reducing goby mortality. Rates of death
are also expected to be alleviated for the shrimp as gobies warn shrimp
when active outside the burrows of the presence of predators through tactile
communication (Karplus, 1979, 1987; Preston, 1978).  erefore, shrimp are
believed to be less vulnerable to predators when paired with a goby.
A laboratory experiment was carried out to determine the impact of
the partnership on rates of growth of both gobies and shrimp forming
an obligatory partnership (Thompson, 2003). Recently recruited gobies
(Ctenogobiops feroculus) and shrimp (Alpheus djeddensis) from a coral reef
lagoon in Moorea, French Polynesia were placed into aquaria containing
optimal substrate (70% sand, 30% rubble;  ompson, 2004). Individuals
were initially measured, weighed and randomly assigned to one of four
treatments: goby alone, shrimp alone, goby plus small shrimp, or goby plus
large shrimp. Individuals in each treatment were fed TetraMin  ake food
and brine shrimp ad libitum. A er 24 days, individuals were reweighed and
572 e Biology of Gobies
it was determined whether growth rates di ered among treatments. Results
showed that shrimp growth was signi cantly greater in treatments where
a goby was present (Figure 4.4.2A). By contrast, there was no di erence
in goby growth between treatments where shrimp were present or absent
(Figure 4.4.2B).  ompson (2003) suggested that shrimp growth rates are
reduced without gobies because shrimp curtail foraging when separated
from their partner. Reduced rates of foraging are known to retard growth
(von Bertalanffy, 1938), which, in turn, reduces reproductive potential.
Gobies, however, continue foraging even if shrimp are absent and hence,
in the absence of predators, there is no impact on goby growth rate by
shrimp. Although this experiment is suggestive of a demographic e ect, the
results must be treated with some caution because it is di cult to perform
an artifact-free laboratory experiment on the goby-shrimp system. For
example, although  ompson (2003) carefully used sediments from the
lagoon (where these goby and shrimp species co-occur), that contained
some natural food, the primary source of food in the experiment was
TetraMin akes that di ered in structure, composition and location from
natural food. Further, although the experimental, the goby and shrimp
seemed to behave normally (despite the absence of predators) with the
shrimp constructing burrows that were occupied by both partners, one
cannot rule out that the shrimp occasionally le the burrows wander to
and feed over the entire aquarium as shrimp o en do in captivity (Karplus,
pers. obs.). Despite the caveats inherent to Thompsons (2003) findings
that the goby impacted the growth rate of shrimp a subsequent  eld study
carried out in Hawaii on A. rapax (Nelson, 2005) seemed to corroborate
Thompson's (2003) results. In this study a shrimp deprived of its fish
partner Psilogobius mainlandi revealed a marked reduction in its foraging
activity compared with an associated shrimp. In addition,  eld observations
in the Red Sea (Magnus, 1967; Karplus, 1987) and the Great Barrier Reef
(Cummins, 1979) suggested that shrimp deprived of their goby shi ed to
a subterranean existence, very likely that the growth of these shrimp was
reduced. Field experiments contrasting the growth of marked associated
shrimp deprived of their goby and in its presence could reveal if gobies
indeed a ect the growth of shrimps.
e impact of the shrimp on goby mortality was assessed through a  eld
experiment in which marked gobies were released into areas of a lagoon in
Moorea containing resident Ctenogobiops feroculus and Alpheus djeddensis
(Thompson, 2005). Prior to goby release, the location of residents was
mapped for a period of approximately two weeks. Upon goby addition,
introduced gobies competed with residents for burrows and 20 of the 48
Ilan Karplus and Andrew Richard  ompson 573
invaders were observed in burrows that previously contained a resident. Of
the remaining 28, none were observed even following extensive searching
of the areas surrounding release.  ompson (2005) interpreted this  nding
to mean that gobies that failed to pair with shrimp were consumed by
predators.
The direct impact of the goby on the shrimp survival is difficult to
evaluate because shrimp deprived of their goby greatly reduce their activity
outside the burrows. Long term monitoring of marked shrimp with and
without gobies in the  eld and of the burrow openings of isolated shrimp
are needed to establish whether shrimp su er from greater predation in the
absence of their  sh partner.
Diet and Feeding Behavior
Little research has been conducted on the diet of various species of
associated gobies and shrimps subsequent to Karpluss (1987) review.
Briefly, gobies of the genera Amblyeleotris, Cryptocentrus, Ctenogobiops
and Vanderhorstia feed by picking organisms directly from the sand as
well as taking mouthfuls of sand and  ltering organisms through their gill
rakers (Magnus, 1967; Hoese and Allen, 1976; Cummins, 1979). Gobies
typically pick through sediment around the burrow entrance and have
been observed to pick through sediment extracted from a burrow by a
shrimp (Hoese and Steene, 1978; A.  ompson, pers. obs.). In addition,
some species such as Amblyeleotris japonica in Japan (Yanagisawa, 1982),
Fig. 4.4.2 The in uence of gobies on the growth rate of their shrimp partners and vice
versa (Error bars depict 1 SE). A. Proportion change in Alpheus djeddensis weight after
24 days in the presence and absence of a Ctenogobiops feroculus. B. Proportion change
in the weight of Ctenogobiops feroculus after 24 days when paired with a large (mean
total length = 53.7 mm) A. djeddensis, small (mean total length = 23.4 mm) A. djeddensis
or when the goby was alone (after Thompson, 2003).
574 e Biology of Gobies
and Stonogobiops xanthorhinica in Papua New Guinea (A.  ompson, pers.
obs.) were observed to ascend approximately 1-5 cm in the water column
and apparently pick at planktonic food items.
Analysis of A. japonica gut contents showed that these gobies consumed
primarily corophiid amphipods and other small species of crustaceans
(Yanagisawa, 1982). Similarly, Cummins (1979) stated that stomach
contents of shrimp-associated gobies found near One Tree Reef in Australia
of the genera Amblyeleotris, Cryptocentrus, Ctenogobiops and Vanderhorstia,
consisted largely of small invertebrates (i.e., amphipods, copepods, bivalves,
and worms), as well as some algae.
Goby-associated shrimps appear to be opportunistic feeders that consume
interstitial matter exhumed during burrow excavation and material such as
algae that is taken when shrimp are outside the burrow. Shrimps in Hawaii
(Moehring, 1972), One Tree Reef (Cummins, 1979) and the Philippines
(Palomar et al., 2004) were all observed taking algae into their burrows.
A recent study using stable isotope analysis of the gut contents of Alpheus
macellarius in the Philippines demonstrated that organic matter from the
sediment and sea grass constitute the majority of the diet of this shrimp.
Furthermore, there was a positive relationship between sediment organic
content and the density of this species (Palomar et al., 2004). In addition,
at least one species of shrimp forages by cleaning its goby partner. Alpheus
djiboutensis was documented inside its burrow placing its  rst set of chelae
on Cryptocentrus cryptocentrus and repeatedly moving its second set of
chelae from the  sh to its mouth (Karplus et al., 1972a).
Habitat Specificity
Several studies indicate that the distribution of goby and shrimp species
is influenced by habitat parameters. For example, Yanagisawa (1984)
demonstrated that Amblyeleotris japonica and Alpheus bellulus in Japan are
found primarily in locations with a mixture of sand, pebbles, coral debris
and shell fragments, but are rarely found in pure-sand habitats. Karplus
et al. (1981) showed that four species of goby-associated shrimps in the
Red Sea inhabit discrete microhabitats that are characterized by depth and
sediment grain size.
More recently, studies in Australia and French Polynesia quantified
habitat associations of shrimp-associated gobies. Thompson (2004)
found that there were non linear relationships between the proportion of
sand, rubble, coral and coral pavement within plots and the density of
Ctenogobiops feroculus that paired with Alpheus djeddensis throughout the
relatively shallow lagoons on the north shore of Moorea, French Polynesia.
Ilan Karplus and Andrew Richard  ompson 575
Speci cally, he found that maximal goby densities occurred in locations
with approximately 70% sand and 30% rubble, and that densities tended
to be low in sites comprised entirely of sand, rubble, coral, or pavement
(Fig. 4.4.3). A laboratory experiment demonstrated that this mixture of
sand and rubble is optimal for burrow construction by A. djeddensis as this
shrimp was unable to construct burrows in pure-sand habitats and relied
on the rubble to buttress tunnels ( ompson 2004; see also section 5 on
burrow structure).  ompson (2004) also found that the three species of
associated gobies and shrimps that are found in Moorea were completely
allopatric and segregated by habitat as C. feroculus and A. djeddensis were
found in shallow, sandy lagoons, Vanderhorstia ornatissima and Alpheus
brevicristatus occurred only in silty, highly protected areas, and Amblyeleotris
fasciata and Alpheus ochrostriatus lived exclusively on the outer reef crest.
Similarly, Syms and Jones (2004) showed that habitat composition dictated
the distribution of multiple shrimp-associated gobies at Lizard Island in
Australias Great Barrier Reef. Here, Vanderhorstia ornatissima was found
Fig. 4.4.3 Ctenogobiops feroculus habitat and density. Scatter plots and best- t trend
lines depicting relationships between habitat and goby density using data calculated at
0.1 intervals bins of each habitat type. Error bars represent 2 SE. Trend lines were used
to t values taken from each bin and were characterized by the following equations: y
= (–)51.86x
3
+ 60.89x
2
– 7.62x + 0.28 (sand), y = 92.28x
3
–152.29x
2
+ 62.29x – 0.06
(rubble), y = 7.27x
2
–13.87x + 6.50 (coral), y = 12.84x
2
–16.89x + 5.40 (pavement), where
y = mean goby density and x = proportion habitat (after Thompson, 2004).
576 e Biology of Gobies
exclusively in the central lagoon and on front reef slopes, Ctenogobiops
pomastictus and C. aurocingulus on reef flats, sheltered back reefs, and
near the lagoon entrance, Cryptocentrus cinctus on the sheltered back reef,
and Amblyeleotris steinitizi on the sheltered back reef and near the lagoon
entrance.
Population Dynamics
Population dynamics of multiple, sympatric species of gobies and shrimps
were studied through a series of observational and manipulative experiments
on One Tree Reef by Cummins (1979). First, censuses of goby and shrimp
abundances at three locations demonstrated that total population size
and relative abundance of particular goby and shrimp species changed
signi cantly through time. Next, Cummins (1979) followed eight di erent
burrows that contained four species of shrimps. Over three observation
periods spanning a period of  ve months, the species of goby occupying
a burrow changed at least once in  ve of the burrows. Finally, Cummins
removed gobies from 14 burrows and found that 12 were recolonized
within three weeks. Of the 12 recolonizations, 10 were by the same species
of goby that was initially removed, one was by a goby that was observed to
commonly associate with that species of shrimp in the  eld, and one was
colonized by a goby that was rarely observed with that species of shrimp.
e latter association, however, was temporary; subsequent observations
demonstrated that this goby abandoned the burrow (see also section below
on partner speci city).
e in uence of biotic factors on shrimp/goby population dynamics were
explored recently in Moorea by  ompson (2005) and in Hawaii by Nelson
(2005).  ompson conducted several observational and  eld experiments
to elucidate the interplay between predation and intraspeci c competition
on Ctenogobiops feroculus populations. First, surveys of sites with habitat
appropriate for C. feroculus/Alpheus djeddenis [a combination of rubble
and sand; see  ompson (2004)] but with variable densities of piscivorous
predators showed that there was no correlation between C. feroculus and
predator densities. Predator density, however, correlated negatively with
the proportion of large C. feroculus and positively with the proportion of
small C. feroculus paired with large shrimp. Next, an experiment in which
tagged C. feroculus were added to several plots demonstrated that 1) these
gobies competed intraspeci cally for burrows, 2) large gobies outcompeted
smaller gobies, and 3) gobies preferred pairing with large as opposed to
small A. djeddensis. Finally,  ompson (2005) experimentally augmented
predator densities by placing roof tiles that attracted ambush predators such
as spotted sandperch (Parapercis millepunctata) on several plots. Although
Ilan Karplus and Andrew Richard  ompson 577
goby mortality increased signi cantly in predator-addition sites relative to
control plots, goby abundance did not change in the predator addition plots.
Rather, gobies that were consumed were replaced quickly by recruits. As
such, the proportion of large gobies per site decreased following predator
addition. Predation, however, seemed to not impact A. djeddensis as the size
structure of shrimp remained unchanged in response to elevated predator
densities.  erefore, the proportion of small gobies paired with large shrimp
increased following predator addition. Nelson (2005) found a very similar
impact of predators on Psilogobius mainlandi and Alpheus rapax in Hawaii.
Rather than attract predators, Nelson (2005) utilized predator exclusion
cages to reduce goby-shrimp exposure to predators. He found that while
goby densities did not change a er  ve months of predator exclusion, there
were more than twice as many large gobies in exclusion plots as compared
to control plots.
BEHAVIOR
Burrow Structure, Construction and Dynamics
e three dimensional subterranean structure of the burrows of associated
alpheid shrimps was revealed with the application of polyester and epoxy
resin casts (Karplus, 1987). Overall, burrows were shallow (not more than
half a meter deep), and in close contact with hard objects such as coral and
rock boulders. Due to the tendency of sand to collapse, hard objects were
used to support the subterranean burrow structure. Sections of the burrows
leading under rocks or corals had chamber-like enlargements whereas casts
retrieved from sediment lacking supporting objects had an even diameter
at di erent points (Fig. 4.4.4B, C).
e e ect of the substratum on burrow structure has been demonstrated
for Alpheus crassimanus (Farrow, 1971). Whereas burrows of this
species that were located in coarse substratum with hard objects had an
irregular structure, those located in muddy/silty substratum had a regular,
dichotomous branching pattern.
Three basic types of burrow openings have been described for Red
Sea associated shrimps including asymmetrical tube, symmetrical tube,
and funnel-like types (Fig. 4.4.4A). Whereas the burrow openings of
all associated shrimps are reinforced by coral and shell fragments, the
subterranean burrow sections of only some of the shrimp species are
reinforced with hard substrates (Cummins, 1979; Karplus, 1987). In
contrast to the lack of species speci city in the structure of the subterranean
burrows, some speci city was revealed in the number (ranging from one to
578 e Biology of Gobies
six) and structure of the burrow openings of Red Sea (Karplus et al., 1974)
and Great Barrier Reef associated shrimps (Cummins, 1979).
The behavior of several species of goby-associated shrimps during
burrow construction has been described in aquaria (Harada, 1969; Karplus
et al., 1972a) and in the sea (Luther, 1958a; Macnae and Kalk, 1962;
Magnus, 1967; Farrow, 1971; Yanagisawa, 1984).  ree di erent digging
techniques have been revealed: 1) Digging with the  rst pair of chelae into
a vertical sand wall and twisting until the sand collapses; 2) Digging with
the second pair of chelae and the third and fourth pairs of periopods; and
3) Digging with the pleopods, mostly practiced inside the burrow. The
transport of sand and small stones from inside the burrow is carried out by
the  rst pair of chelae that are held together to form a  at spade broadened
by rows of long hairs fringing the chelae margins. Occasionally, large,  at
objects such as a shell are grasped by the  rst pair of chelae and li ed up to
reinforce the burrow entrance or used like a tool for more e cient transfer
of sediment (Magnus, 1967; Karplus et al., 1972a).
With very few exceptions, associated gobies rely exclusively on shrimp
to construct burrows. There is only a single report from Aldabra Atoll
of a non-identified goby that participated with Alpheus crassimanus in
burrow construction. Here, the goby enlarged upper parts of the burrow
Fig. 4.4.4 The burrows of alpheid shrimps associated with gobies. A, Three different
types of burrow openings: I. Tube-like symmetrical opening of Alpheus rapax. II. Funnel-
like symmetrical opening of Alpheus rubromaculatus. III. Asymmetrical opening of Alpheus
djiboutensis. B. Epoxy resin cast of the burrow of Alpheus djiboutensis. C. Drawing
indicating the same burrow structure relation to large objects in the sediment (after
Karplus et al., 1974).
Ilan Karplus and Andrew Richard  ompson 579
by removing mouthfuls of mud from within the burrow and ejecting them
at the periphery (Farrow, 1971). By contrast, aquarium-based observations
of several species of associated gobies such as Nes longus (Weiler, 1976),
Cryptocentrus caeruleopunctatus (Magnus, 1967), Amblyeleotris japonica
(Harada, 1969), and Ctenogobiops feroculus ompson (2004) indicated
that these gobies are unable to construct a burrow. When isolated from
shrimp, these species formed a shallow depression by splashing sand that
only provided minimal shelter. It seems that in almost all associations the
burrow is constructed and maintained solely by the shrimp.
Recently, Palomar et al. (2005) studied in the Philippines the behavior
of male Alpheus macellarius associated with Cryptocentrus octafasciatus
in the laboratory under four sediments treatments that differed in the
level of gravel content (0, 5, 15, and 25% gravel) for five consecutive
days. Burrowing was mainly conducted during the  rst day and the early
mornings of subsequent days, thus implying a greater priority for the shrimp
to construct and maintain its burrows relative to other activities. Gravel
content did not signi cantly in uence burrowing behavior, but marked
variations were noted in burrowing success, burrow structure and stability.
Shrimp in 15% and 25% gravel substrates produced larger, more complex
burrows that lasted longer than those of shrimp in 0% and 5% gravel
substrate.  e importance of a high percentage of rubble in the sediment
for optimal burrow construction was also reported for A. djeddensis paired
with Ctenogobiops feroculus ( ompson, 2004).
Daily changes in the position of burrow openings have been reported for
several species and types of associated shrimps (Karplus, 1987). Monitoring
daily changes (i.e., distance and angle) revealed maximal daily shi s of
the opening ranging from 25 to 160 cm; however, the spatial location of
entrances was con ned to a rather limited zone of up to several square
meters (Fig. 4.4.5B). Changes in burrow structure are probably restricted to
the upper, shallow parts of the burrow, whereas the deeper parts that o en
lead under and between large boulders likely remain stable (Karplus et al.,
1974).
Species-speci c trends were found in the daily shi s of the location of
burrow openings of several species and types of shrimp in the northern
Red Sea (Karplus et al., 1974) and the Great Barrier Reef (Cummins, 1979).
ree di erent, non-exclusive mechanisms have been suggested to underlie
the shifting of burrow opening of different associations. First, Magnus
(1967) suggested that the daily changes in the position of the opening
for Alpheus rapax and A. rapacida (both associated with Cryptocentrus
caeruleopunctatus and Vanderhorstia delagoae) resulted from the feeding
580 e Biology of Gobies
Fig. 4.4.5 Multidirectional shifts of the burrow opening due to the combined activities of
goby and shrimp. A. Amblyeleotris steinitzi associated with Alpheus purpurilenticularis.
B. Daily shift in position of burrow opening. Numbers indicate consecutive days. Arrows
indicate location of sand pile in front of burrow opening. C. Dynamics of the upper burrow
system. (a) Goby positioned in front of burrow opening (O1); (b) formation of new burrow
opening (O2) by goby; (c) opening O1 collapsed, new opening functional; (d) formation of
additional opening (O3) by goby; (e) opening O1 and O2 collapsed, opening O3 functional.
(after Karplus et al., 1974).
Ilan Karplus and Andrew Richard  ompson 581
activity of the shrimps.  ese shrimps feed on non-disturbed sediment
overlying the burrow and thus continuously shi the opening backwards.
Second, Cummins (1979) suggested that the  xed changes in the position
of associated shrimp types from the Great Barrier Reef were due to the
digging activity of the shrimps. In this case, both the upper and lower parts
of the burrows were reinforced by coral fragments.  erefore, all parts of
the burrows were stable and the shrimps only alternately cleared or blocked
them with sediment, thus reforming the opening at the same position.
ird, Karplus et al. (1974) suggested that the irregular, multidirectional
shi s in burrow entrances resulted from the combined activities of the goby
Amblyeleotris steinitzi and the shrimp A. purpurilenticularis (Fig. 4.4.5A).
Here, the goby wedges its head through the substratum to create a new
opening and the shrimp follows and enlarges it while the old opening
rapidly collapses (Fig. 4.4.5C).
Daily shi s in the location of burrow openings may be important for
several reasons. First, changing the position of the burrow can continuously
expose shrimps to non-disturbed sediment. Samples of sediments excavated
from the burrows of Alpheus macellarius associated with Cryptocentrus
octafasciatus contained significantly less organic carbon than samples
taken from undisturbed sediments in proximity of the burrows (Palomar,
2001). Because shrimps feed opportunistically on detritus and other items
found in the substrate (Palomar et al., 2005), this may be an important
source of nutrition for the shrimps and may compensate for the limited
exposure to non-disturbed sediment within the relatively shallow burrows.
Second, relocation of burrow entrances may reduce territorial conflicts
among gobies. Con icts between neighbors may be resolved by forming
new openings further away from a nearby, dominant neighbor. Third,
spacing of burrows may alleviate territorial con icts between neighboring
shrimps. Intense  ghting between associated shrimps during paired staged
encounters in the laboratory has been reported for Alpheus rapax and A.
rapacida (both paired with Psilogobius mainlandi) in Hawaii (Moehring,
1972) and between same-sex Alpheus djeddensis in Moorea ( ompson,
2003). Fourth, during the reproductive season of gobies, shifting an
opening towards potential mates could reduce the exposure to predation
when individuals travel between burrows to mate (Karplus et al., 1974).
Activity Rhythms
All studied species of associated gobies and shrimps have demonstrated
a strict diurnal activity rhythm. Both partners remain in their burrows
at night, and the burrow entrances are o en closed due to wave action
or are intentionally sealed o by the shrimp (Yanagisawa, 1984; Karplus,
582 e Biology of Gobies
1987). Activity is renewed by the goby around sunrise as it wedges its head
through the sediment.  e goby is followed very soon a er by its shrimp
partner who enlarges the opening and resumes its activity outside the
burrow. Activity is terminated around sunset by the goby as it retreats into
the burrow. Behavioral changes towards the end of the day were observed
in several shrimp species as they remained outside their burrows for
shorter amounts of time and reinforced the entrances with coral and shell
fragments. Termination of the daily activity is more synchronous than its
onset, probably due to the fact that the end is triggered by low light levels
and the onset more by an endogenous rhythm as levels of light may not be
perceived accurately by the goby and shrimp inside their burrows (Karplus,
1987).
Variation in the daily activity rhythms of several species of associated
shrimps from different localities often revealed a marked increase in
activity in the late a ernoon (Karplus, 1987; Palomar, 2001; Nelson, 2005).
However, maximal activity of several shrimp types in the Great Barrier
Reef occurred at noon (Cummins, 1979). In the Northern Red Sea three
species of associated shrimps (Alpheus djiboutensis, A. rapax and A.
purpurilenticularis) displayed marked variation in mean time spent outside
the burrow during the day that was concomitant with a change in the type
of activity performed. Shrimps activity in the morning mostly consisted
of short exits with chelae loaded with sediment cleared from burrows
that collapsed during the night. In the a ernoon, by contrast, exits were
lengthier, and the shrimps excavated non-disturbed sediment, that was
subsequently transported into the burrow, probably for nocturnal feeding
(Karplus, 1987).
e activity of Alpheus  oridanus was contrasted in southern Florida while
living in association with an obligatory partner (Nes longus), a facultative
partner (Bathygobius curacao) and while free living (Karplus, 1992).  e
shrimp spent  ve fold more time outside the burrow when associated with
the obligatory partner than when associated with the facultative one due to
both more exits per time and increased time spent outside the burrow per
exit (Fig. 4.4.6).  ere was no di erence in the types of activities carried
out over the daily cycle for shrimp with obligatory and facultative partners.
Shrimp associated with the obligatory partner, however, spent more time
picking at plants and digging in sediment than shrimp associated with the
facultative one. Shrimp with the facultative goby engaged almost entirely
in burrow maintenance (e.g. dumping of sediment). Free living shrimp
spent much less time (only about 2%) outside their burrows than any of
the associated shrimp.
The activity of Alpheus rapax outside its burrows in Hawaii while it
was associated with its obligate goby partner, Psilogobius mainlandi, or
Ilan Karplus and Andrew Richard  ompson 583
while it was deprived of its  sh partner was contrasted by Nelson (2005).
Whereas deprived shrimp spent only 7% of the time outside the burrow
(for an average duration of 3 seconds), those with a goby were outside 54%
of the time (for an average of 14 seconds). Deprived shrimp were almost
entirely (98% of the exits) occupied with burrow maintenance activities
such as clearing the burrow of sediment and manipulating rubble around
the burrow entrance, whereas associated individuals carried out burrow
maintenance in only 53% of their exits and spent the rest of their time
conducting other activities such as foraging.
Interspecific Communication
e restrictive conditions for tactile communication (i.e., close proximity
of the communicating parties) are perfectly met in the partnership between
gobies and alpheid shrimps. As long as the shrimp stays outside the burrow
it maintains a continuous antennal contact with its  sh partner (Fig. 4.4.10).
e goby warns the shrimp of danger by two di erent types of warning
signals:
Fig. 4.4.6 Activity of Alpheus oridanus outside its burrow when associated with Nes
longus (obligatory partnership-broken line) and Bathygobius curio (facultative partnership-
continuous line) (after Karplus, 1992).
584 e Biology of Gobies
(1) Tail- icks: rapid, small lateral  n- icks which are only produced
when the shrimp is outside the burrow and o en induce the shrimp
to enter its burrow or “freeze” at the entrance.
(2) Head first entries: rapid head first entries of the goby into the
burrow produced when the shrimp is either present or not outside
the burrow the shrimp always enters the burrow when the goby
enters the burrow head  rst.
e production of warning signals by the goby Amblyeleotris steinitzi was
studied in a shallow lagoon in the northern Red Sea during the a ernoon
when its shrimp partner, Alpheus purpurilenticularis, spent most of its time
outside of the burrow (Karplus, 1979).  e goby generated an average of
7.4 tail- icks per hour. Signals were produced in series (spaced less than
5 s apart) with numbers varying from 1 to 9 and a mean of 1.7 signals per
series. Tail- icks were emitted in response to all approaching large  shes
irrespective of their feeding habits, whereas all small  sh were ignored.
e goby was selective in its response towards approaching medium sized
shes, signaling in response to piscivorus  shes and  shes digging in the
sediments that can block the burrow entrances (e.g. goat sh) but ignoring
medium sized fishes that feed on algae or coral (e.g. surgeon fish and
butter y sh). In a controlled experiment using live  shes presented to the
goby inside a perspex box at a  xed distance from its burrow the di erential
signaling response to a predatory vs. a non predatory  sh was con rmed.
e shrimp retreated into the burrow in response to approximately 60%
of the single signals but to 90% of series composed of these same signals.
Some series of signals that did not induce the shrimps retreat seem to have
been made in situations of little danger (e.g. an intruder already leaving the
burrow vicinity). Head  rst entries by the goby were performed at a rate
of 0.3 times per hour and always caused a rapid retreat of the shrimp into
its burrow.  e same intruding  sh that induced the warning signals also
induced at close range the goby’s head  rst retreat.
Production of tail- ick warning signals by the goby Amblyeleotris steinitzi
in response to the approach of di erently sized two-dimensional predator
models was investigated in the northern Red Sea (Karplus and Ben-Tuvia,
1979).  e distance between the model and the goby at which the goby
entered its burrow head  rst was de ned as the critical point. A negative
correlation was found between the number of tail- icks and the distance
from the critical point.  e occurrence of dynamic  elds of interspeci c
communication around the burrow opening has been suggested. As soon
as a speci c distance (typical for each type of intruding  sh) is crossed and
the shrimp is outside the burrow, the goby begins to  ick its tail, signaling
to the shrimp to enter its burrow.  e rate of signaling increases as the
Ilan Karplus and Andrew Richard  ompson 585
intruder approaches the burrow with the alert goby remaining outside the
burrow and carrying out activities such as foraging. However, as soon as
the intruder reaches the critical point, the goby performs a head  rst entry
either in the presence or absence of the shrimp partner, thus terminating
all activities outside the burrow by both the goby and shrimp.
Due to the speed and complexity of the goby-shrimp tactile
communication, detailed analyses can only be made through the use of video
or  lm recordings. (Karplus et al., 1979; Karplus, 1987). Quanti cation of
lms revealed  ve parameters of the tail- ick signal of Amblyeleotris steinitzi
(e.g. duration and amplitude). Speci cally, the communicative tail- icks
are graded and coded signals that are conspicuously di erent from other
tail movements.  e tail- ick warning signal of this species is shorter than
one second in duration and had a maximal amplitude of less than 1 cm
(Fig. 4.4.7). A principle component factor analysis followed by a stepwise
regression analysis revealed the impact of 18 variables (e.g. shrimp chelae
empty or loaded with sediment, the speed of the shrimp and its direction)
on the shrimp retreat response.  e structure of the preceding and actual
warning signals and the area of contact of the antenna accounted for
approximately a third of the di erences in the shrimps retreat response.
e most important signal variable is the total distance traversed (TDT) by
the caudal  n.
Fig. 4.4.7 Graphical presentation of the interaction between the tail- ick warning signal
of Amblyeleotris steinitzi and the response of its shrimp partner Alpheus purpurilenticularis
(after Karplus et al., 1979).
586 e Biology of Gobies
e feedback mechanism by which the goby regulates the intensity of
the tail- ick warning signals, according to the shrimps response is one of
the most complex aspects of this communication system. If the shrimp does
not respond to its tail- icks, the goby increases the intensity of its signal
(measured by TDT). By contrast, upon the rapid retreat of the shrimp the
sh decreases the signal intensity.  e goby’s regulation of the intensity of
the warning signal according to the shrimps response is possible because
the mean time interval between two consecutive signals of a series (1.6 ±
1.1 s) is signi cantly longer than the mean latency of the shrimps response
(0.5 ± 0.4 s).
When a goby retreats head  rst into a burrow, the shrimp inevitably also
retreats and the movement of both partners is so rapid that only a cloud of
sand can be perceived by the observer. Film analysis revealed that during
the head first entry the goby, which initially was facing away from the
burrow entrance, bends laterally its head, almost touching its tail and then
enters the burrow head  rst. e shrimp latency of response to a head  rst
entry is much shorter (0.16 s) compared with its mean latency of response
to a tail- ick (0.51 ± 0.36 s). Similarly, the mean speed of retreat following a
head  rst entry (93.7 ± 54.9 mm/s) is  ve times more rapid than the mean
retreat speed following a tail- ick (16.5 ± 7.2 mm/s). Because the head  rst
retreat takes place under circumstances of extreme danger such as a direct
predator attack, any delay in the shrimp response may cause it to be killed.
erefore, there was likely a strong selection for rapid response.
e body site of contact between the shrimp and goby di ers according to
the position of the shrimp relative to the goby (Karplus et al., 1979). When
the shrimp was behind the goby, both its antennae pointed forward and one
of them touched the goby’s caudal  n. When the shrimp was parallel to the
goby, one antenna was bent sideways touching the second dorsal  n, while
the other still pointed forward. When the shrimp was further away from
the burrow than the goby, one antenna pointed backwards and touched
the goby’s pectoral fin, while the other was directed forward. Warning
signals are given with various  ns including the caudal, second dorsal, anal
and pectoral  ns according to the area of antennal contact. In each case,
however, the caudal  n is involved in signaling (Fig. 4.4.8).  e possibility
of signaling using several  ns enables the shrimp to move further away
from the goby while still being protected through the warning system.
Ilan Karplus and Andrew Richard  ompson 587
Fig. 4.4.8 Fins of Amblyeleotris steinitzi taking part in signaling (left side) and the areas
of antennal contact (right side-stippled). C = caudal n; A = anal n; D2 = second dorsal
n; D1 = rst dorsal n; P = pectoral n (after Karplus et al., 1979).
The importance of the antennal contact for the transmission of
information in the goby-shrimp partnership was revealed in observations
on A. djiboutensis with a single partially ablated antenna (Karplus et al.,
1972a). Without the antennal contact the shrimp did not respond to the
head  rst retreat of its partner Cryptocentrus cryptocentrus which would
normally result in its rapid withdrawal.
Differences in the response of two shrimp species found in Hawaii,
Alpheus rapax and A. rapacida, that both pair with Psilogobius mainlandi
is probably related to di erences in length of their antenna (Preston, 1978).
On the one hand, A. rapax, which has long antennae, can dig at a relatively
far distance from the goby and still maintain contact with the  sh. Alpheus
588 e Biology of Gobies
rapax is capable of di erentiating between generalized goby movements
and tail  ick signals (Preston, 1978). On the other hand, the relatively short
antennaed A. rapacida maintains more body contact with the goby and
usually cannot distinguish between generalized and specialized movements
of the goby.
Over the last twenty years research on interspecific communication
has focused mainly on Atlantic species.  is work has contributed to our
understanding of the possible evolution of these associations by studying
both obligatory and facultative partners (Karplus, 1992; Randall et al.,
2005). In a  eld study carried out in southern Florida, the facultative shrimp
partner Alpheus floridanus maintained antennal contact with both its
obligatory  sh partner, Nes longus, and its facultative partner, Bathytgobius
curacao. Occasionally, however, contact was not maintained when the
partners were within a distance of several centimeters and the goby’s body
was located between the le and right shrimps antenna (Karplus, 1992).
In contrast, no antennal or incidental contact was maintained by the
same shrimp species when associated with another species of facultative
sh partner, Ctenogobius saepepallens, in Belize (Randall et al., 2005). In
obligatory Indo-Paci c associations the antennal contact between goby and
shrimp is continuous when they are close to each other. Only when the
goby is positioned at the far end of a long furrow (leading in a straight line
to the burrow opening) does the shrimp venture out of its burrow without
antennal contact. However, also under these circumstances the shrimp is
still protected by the goby since the same furrow that is used by the shrimp
when leaving the burrow, is also used by the goby as its escape route, such
that the goby collides with the shrimp when rushing into the burrow.
Obligatory and facultative fish partners in southern Florida differed
markedly in the types of warning signals they produced to warn their shrimp
partner, Alpheus  oridanus (Karplus, 1992). Whereas the facultative  sh
partner Bathygobius curacao produced only head  rst entries, the obligatory
partner Nes longus produced both head  rst entries and rapid tail- icks.  e
latter warning signals resemble those described for obligatory Indo-Paci c
sh partners.  e generation of warning signals by Nes longus associated
with A.  oridanus was studied in the laboratory with a  lm camera and
a motor driven three dimensional barracuda model. Preliminary analysis
of the video revealed an increase in the rate of signaling as the model
approached the critical point, followed by a head  rst retreat of the goby
(Karplus, unpublished data). One of the important di erences between the
obligatory partner, Nes longus, and the facultative Bathygobius curacao is
related to the way the goby positions itself at the burrow entrance. Whereas
Nes longus always positioned itself in the activity zone of the shrimp with
Ilan Karplus and Andrew Richard  ompson 589
its tail directed towards the opening, Bathygobius caracao positioned itself
in the shrimp activity zone during only 40% of the observations and its tail
typically was not directed towards the entrance (Fig. 4.4.9).  erefore, the
shrimp was likely much more aware of the obligate than the facultative goby.
Aborted exits (i.e., exits of shrimp terminated by a retreat when no contact
is made with the goby) were  ve times more common in associations with
the facultative sh partner and o en occurred when the goby was in the
vicinity of the burrow. When associated with an obligate partner, aborted
exits only occurred when the goby was absent from the entrance area
(Karplus, 1992).
The study of the communication between Lotilia graciliosa and the
shrimp A. rubromaculatus (Fig. 4.4.10C) is of special interest because of the
extreme partner speci city in this obligatory association and the habit of
this goby to hover above the burrow opening (most associated gobies perch
on the sediment in front of the burrows).  e di culty in studying this shy
goby was overcome by installing a remote controlled video camera in front
of the burrow that was connected to a monitor and recorder on shore. In
this obligatory, Indo-Paci c association, the shrimp maintains continuous
antennal contact with the goby while outside the burrow.  e goby does
not produce any tail- icks but warns its shrimp exclusively by head  rst
and tail  rst burrow entries.  e frequency of these signals is much higher
than in gobies that produce both tail-flick and burrow entry warning
signals. Both goby and shrimp stay close to the burrow opening. Shrimp
activities are restricted to burrow maintenance and some feeding near the
burrow entrance with little introduction of sediment for nocturnal feeding.
e greater reliance of this shrimp on subterraneous food may be related
to its deeper burrow.  e unique partner speci city in this association is
probably related to a di erent interspeci c communication system (Karplus
et al., 2002; Karplus, in preparation).
Reproduction
At present only a single study in Japan addressed the important issues
of reproduction and the early formation of the goby-shrimp partnership
(Yanagisawa, 1982, 1984). Yangisawa monitored over extended periods of
time marked individuals of Amblyeleotris japonica and its shrimp partner
Alpheus bellulus. In this relatively high-latitude system, which is characterized
by distinct seasonal  uctuation in water temperature, male gobies form
pairs with females from May to September by moving cautiously over
the substratum and rarely venturing more than 3 m from their burrows.
Females were rather passive and sometimes refuse to pair with wandering
590 e Biology of Gobies
Fig. 4.4.9 A. Shematic view of the area surrounding the burrow entrance of Alpheus
oridanus. B. Position of Bathygobius curacao at the burrow entrance. C. Orientation
of Bathygobius curacao to the burrow entrance while in the shrimp activity zone (after
Karplus, 1992).
Ilan Karplus and Andrew Richard  ompson 591
Fig. 4.4.10 Associations between gobies and alpheid shrimps from the Indo-Paci c
region. A. Stonogobiops xanthorhinica and Alpheus randalli, Japan, (Photo: T. Hirata).
B. Amblyeleotris wheeleri and Alpheus ochrostriatus, Japan, (Photo: T. Hirata). C. Lotilia
graciliosa and Alpheus rubromaculatus (Photo: P. Nahke). D. Cryptocentrus maudae and
Alpheus sp. Bali, Indonesia, (Photo: R. Steene). Note the bright color of both gobies and
shrimps and the antennal contact between the partners.
Color image of this gure appears in the color plate section at the end of the book.
males. Paired males were sometimes attacked and replaced by other males.
e strong competition in this species may be accounted for by the fact
that only a small percentage of females were gravid at one time while
most adult males were apparently sexually active throughout the breeding
season. At most only about 7% of all shrimp burrows contained pairs of
gobies during July and August, and males typically paired with a female
only once during the breeding season. Established pairs were maintained
for several days. A 77-mm female was observed to lay in captivity an egg
mass containing about 20,000 eggs. A er spawning, females either leave
the burrow or position themselves at the entrance while the males spend
from four to seven days inside the burrow taking care of the eggs until they
hatch.
Most Alpheus bellulus burrows are inhabited by a stable, heterosexual
pair.  e size of the two genders is positively correlated, although in adult
pairs females are slightly larger than males.  e proportion of ovigerous
females was highest from mid July to mid August.  e number of eggs
carried by a female was positively correlated with her size and its maximal
recorded number was close to 4500. Juvenile shrimp settle on the substrate
Color
592 e Biology of Gobies
from late July to early October. ey mature and reproduce within one
year of settlement. At the onset of their benthic lives they are single, but
gradually form pairs, with 50% already paired four to six months after
settlement but prior to sexual maturation.  e shrimp probably acquire
mates subterraneously when their burrows merge.
Yanagisawa (1982, 1984) suggested that the post larval shrimp starts
digging a small burrow as soon as it settles to the bottom. Following
settlement to the benthic environment, a juvenile goby exploring the
bottom may encounter such a burrow and form a partnership with its
occupant.  e establishment of the association as early as possible a er
settlement is essential to avoid predation (e.g. a shrimp with a carapace
length of 1.7 mm was observed associated with a goby 8.7 mm standard
length). When the burrows of two shrimp merge and they form a pair, the
smaller of the two gobies is forced to abandon the burrow by the larger
one. Many of the evicted gobies are lost to predation, resulting in strong
density-dependent mortality of juvenile gobies.
Partner Specificity
e occurrence of several di erent species of associated alpheid shrimps
and gobiid  shes in the same area poses several questions with respect to
the degree of partner speci city, its regulating mechanisms, and functions.
Early studies on partner speci city simply noted the occurrence or non-
occurrence of certain species of gobies and shrimps in the same burrow
(Harada, 1972; Polunin and Lubbock, 1977; Nakasone and Manthachitra,
1986). Using occurrence vs. non-occurrence as the sole criteria for
speci city, however, could be misleading since the association composition
could result from random independent distribution of both species over
burrows.  e rst quantitative study on partner speci city was carried out
by Cummins (1979) on six species of gobies and four types of shrimps in
the sandy lagoon of One Tree Reef in the Great Barrier Reef, Australia.
Chi-square analysis was used to determine whether the distribution of
goby species across types of shrimp di ered signi cantly from random.
ree species of gobies were associated both as juveniles and adults with
a single “preferred” type of shrimp, while in one species of Amblyeleotris
only the adults were partner speci c. One species of goby was equally and
signi cantly more associated with two types of shrimps and another species
was associated at random with all four types of shrimps.
The most detailed study to date on partner specificity utilized a
combination of  eld and laboratory studies to discern patterns among Red
Sea goby-shrimp associations (Karplus et al., 1972b, 1974, 1981; Karplus,
Ilan Karplus and Andrew Richard  ompson 593
1981). The following three questions were addressed by analyzing the
composition of over 750 associations: (1) Does a species of goby occur
together with a species of shrimp in the same burrow?; (2) Is the number of
co-occurrences signi cantly di erent (more or less) than would be expected
from a random distribution of both species over burrows?; and (3) What is
the strength of the association between two species, measured using Pielou’s
(1969) correlation coefficient? Three different types of specificity were
found in shallow water where four di erent species of shrimps occupied
di erent microhabitats: Type I) Co-occurrences of goby and shrimp species
in the same burrow, with a signi cant positive correlation coe cient; Type
II) Co-occurrences of goby and shrimp species in the same burrow, with a
signi cant negative correlation coe cient; and Type III) no co-occurrence
of goby and shrimp species in the same burrow, and a negative correlation
coe cient. In the shallow water each shrimp species had a strong association
with a single species of goby of a di erent genus. In deep water each of the
species of shrimp occupied the same habitat and no partner speci city was
revealed (Fig. 4.4.11).
Laboratory observations revealed that both gobies and shrimps
exhibit strong, negative phototactic responses as well as strong, positive
thigmotaxis (touch-based orientation) (Karplus et al., 1972b). Laboratory
experiments also revealed a mutual attraction between certain species of
gobies and shrimps based on di erent sensory modalities.  e gobies are
visually attracted to speci c species of shrimp which have distinct colors
and patterns (Fig. 4.4.10). Shrimps, by contrast, are chemically attracted to
speci c gobies (Fig. 4.4.12; Karplus et al., 1972b; Karplus, 1981).  e three
major mechanisms that regulate partner speci city are the attraction of the
goby to the shrimps burrow, the formation of the tactile communication
system and the mutual attraction of goby–shrimp pairs.  e presence or
absence of each of these mechanisms determines the type of speci city of
a speci c goby and shrimp. In Type I partnerships, the goby is attracted
to the shrimps burrow, the tactile communication is formed and the
goby and shrimp are mutually attracted.  ese associations are common,
stable and have been observed for long periods of time (i.e., months). In
Type II partnerships, the goby is attracted to the shrimps burrow, the
tactile communication is formed but there is no mutual attraction.  ese
associations are rare and unstable lasting for relative short periods of time
(i.e., days or a few weeks). In Type III partnerships, the goby is attracted to
the shrimps burrow, the tactile communication system is not formed and
the goby and shrimp are not mutually attracted.  ese associations are not
found in the sea and cannot be formed in the laboratory.
594 e Biology of Gobies
e shrimps plays an active role in determining its partner’s identity.
Shrimps deprived of their goby partners o en block the burrow openings
and leave only a small aperture. Gobies seeking shelter in a shrimps burrow
insert their tail into that opening.  e shrimp readily touches the goby’s tail
with its antenna. If the goby is a preferred species, the opening is enlarged
and the goby is allowed to enter (Karplus et al., 1981). If the goby is not
preferred by the shrimp, an association may not form. For example, in
the laboratory it was not possible to form an association between Alpheus
purpurilenticularis and Cryptocentrus lutheri which are not found to be
associated in the sea. During an entire month the shrimp avoided any
antennal contact with this species of goby. Replacement of C. lutheri by
the “preferred” goby (Amblyeleotris steinitzi) resulted in the immediate
formation of the antennal contact and response of the shrimp to the goby’s
Fig. 4.4.11 Diagramatic presentation of the strength of the associations between gobiid
shes and alpheid shrimps in the northern Red Sea (Eilat Nature Reserve): black lines-
more frequent than random co-occurrences of goby and shrimp in the same burrows,
a signi cant positive correlation coef cient, with the width of the line representing the
strength of the association; white lines-less frequent than random co-occurrences of goby
and shrimp in the same burrows, a signi cant negative correlation coef cient; stippled
lines- independent co-occurrences of goby and shrimp in the same burrows (after Karplus
et al.,1981).
Ilan Karplus and Andrew Richard  ompson 595
tail- ick warning signals.  e actual formation of a speci c association is
probably much more complex than suggested. In addition to the attraction
to the burrow and the shrimp, the goby may also be attracted to a speci c
microhabitat and a species-speci c burrow entrance structure (Fig. 4.4.4A).
Fig. 4.4.12 A. Apparatus for testing the chemical attraction between gobies and their
shrimp partners; B. the flow pattern of stained water within the Y-channel; a-water
reservoir; b-connecting plastic tube; c-regulation clamp; d-bifurcation clamp; e-cells for
holding gobies or shrimp; f-perforated partitions; g-partition regulating water level; h-arm
of Y channel; i-stem of Y-channel; j-removable net partition; k-non-removable net partition;
l-exit of water (after Karplus, 1981).
596 e Biology of Gobies
Interspecific competition among gobies over shrimp burrows may also
a ect the identity of goby-shrimp partners.
Preference of the goby for some traits of the burrow such as size and
stability may a ect partner speci city. Species of large gobies were associated
at One Tree Reef, Australia with large types of shrimp that construct large
burrows (Cummins, 1979). At Palau, mature males of the dominant goby
species Cryptocentrus singapurensis select the burrows of Alpheus macellarius
out of  ve types of shrimp probably because A. macellarius construct very
stable burrows which may enhance spawning success. Juveniles and females
of this species of goby occupied the burrows of all  ve shrimp types (Sakaue
et al., 2005).
e most intriguing and least understood aspect of partner speci city is
probably the way it is related to the goby-shrimp communication. Polunin
and Lubbock (1977) suggested that a species-specific communication
system between goby and shrimp species would enhance communication
e cacy but reduce the number of available hosts whereas a non-speci c
communication system could have lower transmission efficiency but a
higher number of potential partners. Although species-speci c di erences
in communication systems of several Red Sea associations were found
(Karplus, 1976, 1987, 2005), more detailed studies are required to better
understand the role interspeci c communication plays in the regulation
of partner specificity. Some insight may be gained from the obligatory
association between Lotilia graciliosa and Alpheus rubromaculatus (Fig.
4.4.10C). In this association, extreme partner speci city occurs together
with a unique communication system based entirely on head  rst and tail
rst burrow entries and lack of tail- icks that is common in other species
(Karplus, 1987, 2005; Karplus et al. 2002).
GOBY-SHRIMP PHYLOGEOGRAPHY
A recent study examined dispersal dynamics of associated gobies and
shrimp.  ompson et al. (2005) used mitochondrial DNA to examine the
phylogeography of the  erce shrimp goby, Ctenogobiops feroculus and the
shrimp, Alpheus djeddensis. Both of these species have planktonic larvae and
hence harbor the potential to disperse signi cant distances from their place
of birth (Caley et al., 1996). Female shrimp brood eggs that are released
into the water column upon hatching (A.  ompson, unpublished data).
Although the reproductive mechanisms have not been studied speci cally
for C. feroculus, plankton tows within a lagoon in Moorea collected larvae
of this species (A.  ompson and C.  acker, unpublished data).  ompson
Ilan Karplus and Andrew Richard  ompson 597
et al. (2005) tested the hypothesis that both C. feroculus and A. djeddensis
exhibit similar patterns of gene  ow and colonization dynamics.
Thompson et al.s (2005) study focused on the central-eastern South
Paci c. Between 11 and 27 individual Ctenogobiops feroculus and Alpheus
djeddensis were collected from Fiji, Rarotonga (Cook Islands), Rangiroa
(Tuamotu Islands), Moorea, Raitea, Huahine and Bora Bora (Society
Islands). Ctenogobiops feroculus and A. djeddensis were the only mutualistic
goby and shrimp taxa found in the lagoons of islands east of Fiji. In Fiji,
however, A. djeddensis paired with Ambleleotris steinitzi as well as C.
feroculus. Genetic analyses based on 997 and 348 base-pairs of mitochondrial
cytochrome b from C. feroculus and A. djeddensis, respectively, provided
several important findings. First, shrimp grouped into multiple clades
unrelated to geography.  is result was interpreted to mean that the shrimp
recognized as A. djeddensis may actually have been comprised of more than
one, cryptic species. Cryptic speciation is known to be common in alpheid
shrimps (Mathews, 2006) and this result underscores the need for more
research on the taxonomy of alpheid shrimp (see Systematics section of this
review). Gobies and shrimp from the most common clade (two-thirds of
the sampled individuals fell into this clade), exhibited very similar genetic
patterns. First, genetic signatures were signi cantly di erent between Fiji
and all other sample locations, but did not di er signi cantly among any
other populations. Second, isolation-by-distance slopes (a measure of
genetic versus geographic di erentiation for pairs of sample locations) were
almost identical for gobies and shrimp (Figure 4.4.13). Isolation by distance
slopes are o en used to infer mean dispersal distances for aquatic species
(Palumbi, 2003); thus it is probably that C. feroculus and A. djeddensis have
very similar dispersal potentials.
e nding that these species exhibit similar patterns of dispersal has
implications for the ability of these species to colonize habitats. Because
Ctenogobiops feroculus and Alpheus djeddensis pair exclusively with each
other in the eastern South Paci c, successful colonization of empty habitats
in this region likely depends on the near-simultaneous arrival of individuals
from both species. If one species disperses a greater distance than the other,
then mortality rates of the long-distance disperser may be greater than the
short-distance disperser if the former settles in locations where its partner
is not present. Hence, congruent dispersal distances may depict the optimal
strategy for pairs of gobies and shrimp to colonize new habitats.
Indeed, ompson et al. (2005) found that intra-site genetic variability
was lower for both species in the eastern than in the western islands
598 e Biology of Gobies
and that there was a signi cant, positive relationship between goby and
shrimp inter-site genetic variability among islands (Fig. 4.4.14).  is result
was interpreted to mean that eastern populations were founded more
recently than those in the west. A potential reason for eastward population
expansion is that the eastern islands are volcanic whereas many in the
west are part of continental plates. Volcanic islands such as Moorea are
characterized by narrow, shallow lagoons surrounded by steep-sloped reef
crests. On continental plates, by contrast, the drop o from a lagoon to
the reef crest is much less steep. Thus, lagoons on volcanic islands are
extremely vulnerable to drops in sea level, and there is strong evidence that
these lagoons dried out during periods of low sea level associated with the
last ice-age (approximately 14 000 years ago).  erefore, ompson et al.s
(2005) results suggest that Ctenogobiops feroculus and Alpheus djeddensis
colonized eastern Paci c islands by dispersing in tandem from western
islands that were more likely to persist during periods of low sea level.
EVOLUTION
Complex, obligatory associations may have evolved from loose, facultative
partnerships. Such a facultative relationship was described for Ptereleotris
hanae and Alpheus bellulus in Japan.  is hovering goby occasionally takes
shelter in shrimp burrows thereby warning the shrimp in case of danger by
its head  rst entry (Yanagisawa, 1978). A similar relationship was recently
Fig. 4.4.13 Isolation by distance plots for A. C. feroculus (y = 0.0002x – 0.06) and B.
clade 1 A. djeddensis (y = 0.0002x – 0.06). Geographic distances are based on straight-
line separation between sample locations (after Thompson et al., 2005).
Ilan Karplus and Andrew Richard  ompson 599
Fig. 4.4.14 Nucleotide (π) diversities as a function of longitude for A. Ctenogobiops
feroculus (r
2
= 0.95, y = –0.00006 + 0.014) and B. A. djeddensis (r
2
= 0.53, y = –0.00016x
+ 0.044). Triangles depict samples from Okinawa, squares from Fiji, diamonds from the
Cook Islands, and circles from French Polynesia (after Thompson et al., 2005).
described in the western Atlantic between the facultative non-hovering
Ctenogobius saepepallens and A.  oridanus (Randall et al., 2005; Kramer et
al., 2009). Antennal contacts were gradually established by the shrimp with
gobies entering their burrows.  e poor vision of the subterranean shrimp
(Luther, 1958; Magnus, 1967) probably facilitated the evolution of this
tactile communication system between shrimp and goby. An interspecifc
comparison of the visual system of free living alpheids and alpheid shrimp
associated with gobies is still lacking. Causual observations in aquaria on
associated Indo-Paci c shrimp suddenly isolated from their  sh partner
indicated that they were largely disoriented and did not respond to the
approach of a rod. In the eld, isolated shrimp walked straight into a jar
that was hold by a diver (Karplus, pers. observ.).  e initial purpose of the
antennal contact was probably only to inform the shrimp an interspecifc
comparison of the visual system of free living alpheids and alpheid shrimp
associated with gobies is still lacking. Causual observations in aquaria on
associated Indo-Paci c shrimp suddenly isolated from their  sh partner
indicated that they were largely disoriented and did not respond to the
approach of a rod. In the eld, isolated shrimp walked straight into a jar
that was hold by a diver (Karplus, pers. observ.) of the goby’s presence
at the entrance, with the goby retreat into the burrow being the only
warning signal. Such a relationship has been described for Bathygobius
curacao associated with A.  oridanus (Karplus, 1992). Concomitant with
the formation of the antennal contact with the goby the shrimp may have
begun to spend more time outside its burrow (Karplus, 1992). Magnus
600 e Biology of Gobies
(1967) and Preston (1978) both suggested that the specialized tail-flick
warning signals evolved from intentional movements of the goby related
with its retreat into the burrow. An intermediate phase in the formation
of the ritualized tail- icks is the wide amplitude tail-beat.  e tail-beat is
still the dominant warning signal in the Hawaiian shrimp goby Psilogobius
mainlandi, produced in cases of higher danger than the tail-flick. In
Amblyeleotris steinitzi, the tail-beat signal is seldom emitted and only
under conditions of heavy body contact. In this species the tail- ick is the
dominant signal—e ective, economic, graded and coded, a signal produced
at a low amplitude and short duration.
e obligatory associations between burrowing alpheid shrimp and non-
burrowing gobiid  shes are among the few mutualistic marine associations
that very likely have co-evolved.  e complex tactile communication system
between gobies and shrimps, including the unique feed-back mechanism,
has clearly co-evolved. Similarly the mutual attraction between gobies
and shrimps based on di erent sensory modalities could only evolve with
these two organisms in close association.  e bright colors of many of the
di erent shrimp species and types (Fig. 4.4.10) are probably used for their
selection by their “preferred” gobiid partner since the shrimps themselves
are almost blind. Additional aspects of the associated goby and shrimp
biology, such as their intervened activity rhythms and their synchronized
breeding season reflect a complex co-evolutionary history. There is no
doubt that the many diverse interrelated and elaborate adaptations which
resulted from the association between gobies and shrimp provide both of
them with advantages over their free-living relatives that are re ected in
their richness in species, wide distribution and abundance.
Given the complex nature of the interactions between gobies and
shrimps, an important evolutionary question is whether all associated
species evolved from a single common ancestor or if the interaction evolved
independently on multiple occasions. Preliminary phylogenetic analyses
based on the mitochondrial ND2 gene indicate that the interaction evolved
more than once. Within a consensus tree derived from parsimony analysis
that included 27 species of non associated gobies and 7 genera of shrimp
gobies, species in the genera Amblyeleotris, Ctenogobiops, and Vanderhorstia
formed a well-de ned clade that separated from a clade containing species
within Cryptocentrus, Tomiyamichthys, Stonogobiops and Mahidolia ( acker
and  ompson, in preparation). Similar to the shrimp gobies, preliminary
results based on the mitochondrial CO1 gene using seven species of non
associated shrimps that were analyzed by Williams et al. (2001) and ten
species of goby-associated alpeheids indicated that goby-associate alpheid
shrimps are not monophyletic. Rather, a non-associated species, Alpheus
Ilan Karplus and Andrew Richard  ompson 601
cristulifrons was nested within one of the clades of associated shrimp
( acker and  ompson, in preparation). Further analysis is needed to
better de ne the evolution of both gobies and shrimp.
CONCLUSIONS AND FUTURE RESEARCH
There has been considerable progress in the study of goby-shrimp
associations over the last twenty years. Close to forty new species of
associated gobies have been described. A better understanding of the
dynamic feeding behavior of associated shrimp was gained by combining
research with stable isotopes with stomach content analysis.  e use of
remote controlled video cameras allowed the reliable study of goby-shrimp
communication systems. In addition, carefully controlled observational
and manipulative experiments examined the population dynamics of
gobies and shrimp in multiple geographic locations. Recent application of
mitochondrial DNA analysis elucidated the so far completely unknown
dispersion potential, colonization patterns and evolution of both gobies and
shrimps.
Our study of the goby-shrimp partnership is only at its very beginning.
Only the morphology is known for most described species and nothing
about their behavior and ecology. It is currently also clear that goby-shrimp
associations are far from being uniform di ering in many aspects of their
co-evolved biology.  roughout the text of this review many areas that
need further research have been emphasized. However, some of the most
intriguing and complex questions that should be addressed are related to
the mechanism, function and evolution of partner speci city. Such research
should be interdisciplinary, combining taxonomical, molecular, behavioral
and ecological studies.
ACKNOWLEDGEMENTS
Many thanks are due to Profs. L. Fishelson, J.E. Randall, C.  acker and Dr.
A. Barki for their valuable comments on the manuscript. We wish to thank
Daniel Karplus for the preparations of the  gures. We also wish to thank
Roger Steene and Tomonori Hirata for allowing us to use their photos. We
are grateful to the following publishers: Elsevier, Wiley-Blackwell, Springer
Science + Business Media and Balban for allowing us to use again our
gures rst published in their journals. We are very grateful to Helmut
Debelius for allowing us to use the photo of Lotilia graciliosa (photo Rippel/
IKAN).
602 e Biology of Gobies
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