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How stable are the reef odorpreferences of settling reef fish larvae?Vanessa C. Miller-Sims a b , Jelle Atema a , Gabriele Gerlach c &Michael J. Kingsford da Boston University Marine Program, Biology Department, 5Cummington Street, Boston, MA 02215, USAb University of Southern California, 3641 Watt Way, HNB 218, LosAngeles, CA 90089, USAc Carl von Ossietzky University of Oldenburg, 26131 Oldenburg,Germanyd ARC Centre of Excellence for Coral Reef Studies and School ofMarine and Tropical Biology, James Cook University, Townsville,QLD 4811, Australia
Available online: 1 January 2011
To cite this article: Vanessa C. Miller-Sims, Jelle Atema, Gabriele Gerlach & Michael J. Kingsford(2011): How stable are the reef odor preferences of settling reef fish larvae?, Marine andFreshwater Behaviour and Physiology, DOI:10.1080/10236244.2011.587239
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Marine and Freshwater Behaviour and Physiology2011, 1–9, iFirst
How stable are the reef odor preferences of settling reef fish larvae?
Vanessa C. Miller-Simsa,b*, Jelle Atemaa, Gabriele Gerlachc
and Michael J. Kingsfordd
aBoston University Marine Program, Biology Department, 5 Cummington Street, BostonMA 02215, USA; bUniversity of Southern California, 3641 Watt Way, HNB 218,Los Angeles, CA 90089, USA; cCarl von Ossietzky University of Oldenburg, 26131Oldenburg, Germany; dARC Centre of Excellence for Coral Reef Studies and School ofMarine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia
(Received 29 December 2010; final version received 1 May 2011)
Settlement-stage larvae of the coral reef fishes Ostorhinchus doederleini(Apogonidae) and Pomacentrus coelestis (Pomacentridae) prefer the odorof their settlement reef to that of other nearby reefs. It was unknownwhether these olfactory preferences are temporally stable or the result ofrecent olfactory experience. Ostorhinchus doederleini and P. coelestis larvaewere held in aquaria and exposed to water from either their settlement reefor a neighboring reef for 5–9 days and their olfactory preference was tested.We show that exposure to water from another reef did not influenceolfactory preference. Ostorhinchus doederleini olfactory preference declinedslightly over time whereas P. coelestis preference was gradually lost after2–3 days in captivity. Neither species switched their preference to the newreef odor. While we cannot determine conclusively the time window of odorlearning, imprinting at or shortly after birth is logical and has beendemonstrated in other fish species.
Keywords: reef-fish; Ostorhinchus doederleini; apogonidae; Pomacentruscoelestis; Pomacentridae; larval behavior; olfaction; dispersal
Introduction
Most coral reef fish have a pelagic larval dispersal phase after which they must returnand settle on an appropriate reef habitat. Larval fish are not passive throughout thelarval period; late-stage larvae are good swimmers with developed sensory systems(Leis and Carson-Ewart 1997; Stobutzki and Bellwood 1997; Leis and Carson-Ewart1998; Atema et al. 2002; Kingsford et al. 2002; Fisher 2005) and settling reef fishcould influence their own recruitment to reefs either through reef-directed horizontalswimming or by using sensory cues such as odor to choose their position in the watercolumn thus deciding which current to ride. Realistic models show that both of thesemechanisms could facilitate settlement (Wolanski et al. 1997; Armsworth 2000;Armsworth 2001; Cowen et al. 2006). Studies of several species of reef fishdemonstrate that a significant proportion of larvae return and settle on their natalreefs (Jones et al. 1999; Swearer et al. 1999; Cowen et al. 2000; Jones et al. 2005;Almany et al. 2007). Such natal retention is likely enhanced by larval behavior
*Corresponding author. Email: [email protected]
ISSN 1023–6244 print/ISSN 1029–0362 online
� 2011 Taylor & Francis
DOI: 10.1080/10236244.2011.587239
http://www.informaworld.com
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guided by environmental sensory cues, including olfaction (Atema et al. 2002). Atsettlement several species of reef fish are able to use the odor of conspecifics and/ortheir preferred benthic substrate (i.e., coral, anemones, seagrass, leaves) to choose aspecific site on the reef and potentially could use similar cues to locate and swimtoward reefs at the end of the larval stage (Sweatman 1988; Elliott et al. 1995;Arvedlund and Nielsen 1996; Arvedlund et al. 2000a; Lecchini et al. 2005; Dixsonet al. 2008).
We have previously studied the dispersal patterns and olfactory preferences oftwo species of reef fish, the cardinalfish Ostorhinchus (formerly Apogon) doederleiniand the neon damselfish Pomacentrus coelestis, in the Capricorn/Bunker reef groupof the southern Great Barrier Reef (Gerlach et al. 2007). Settlement stage reef fishlarvae are able to use olfaction to detect the odor of a reef. Ostorhinchus doederleini,P. coelestis and several other species of apogonid and pomacentrid larvae prefer thesmell of water collected from a reef to that of open ocean water (Atema et al. 2002).Both species can also distinguish between reefs within the Capricorn/Bunker reefgroup and prefer the smell of water from the reef where they were caught to that ofother nearby reefs (Gerlach et al. 2007). Although both species disperse for similaramounts of time and our test animals dispersed in the same hydrodynamic regime,genetic analysis with microsatellite markers showed limited gene flow between reefsseparated by as little as a few kilometers for O. doederleini but not P. coelestis(Gerlach et al. 2007). Their difference in realized dispersal suggests that behavioraldifferences between these two species influence dispersal.
It has been shown that settlement stage larval reef fish prefer the odor of the reefon which they are settling over that of other nearby reefs, however, it is not knownwhether they are expressing a specific preference for a particular reef or are merelyshowing a preference for the water that they have been exposed to most recently.This study tests between these two possibilities by exposing larvae settling on OneTree Reef to reef water from either One Tree Reef or Heron Reef. If olfactorypreferences are based on recent familiarity then larvae collected on One Tree andexposed to Heron water should change their preference over time to prefer Heronreef water. Stable olfactory preferences should not be influenced by exposure towater from another reef.
Methods
All experiments were performed at the One Tree Island research station between 19January and 9 February 2006 and between 30 January and 6 February 2007. OneTree Island is located in the Capricorn/Bunker Group on the southern end of theGreat Barrier Reef, Australia (23� 300S, 152�E). We collected larvae in the process ofsettling and tested their olfactory preferences; we could not test earlier pre-settlementstages of larvae, which might express stronger or weaker olfactory preference.Settling reef fish larvae were collected daily using three methods. (1) Larvae werecaught in crest nets (0.5mm mesh, 0.5m2 mouth) set in the ‘‘gutter,’’ a tidal channelthrough which during the night high tide settlement-stage apogonids of varyingspecies flood into the lagoon (Finn and Kingsford 1996). (2) Four patch reefs(approximately 100� 100� 50 cm3) were constructed from dead coral rubblecollected from the beach and placed on the sandy bottom of ‘‘shark alley,’’ anotherinflow channel for flood water into the lagoon of One Tree Reef. The patch reefs
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were checked early each day for O. doederleini, Cheilodipterus quinquelineatus, and
Apogon properuptus larvae that had settled there during the night. Animals were
collected from the patch by divers using hand nets. (3) Light traps set outside the
main entrance of the One Tree lagoon were used to collect P. coelestis larvae
(Doherty et al. 1996).Reef water for the larval acclimation and olfactory discrimination tests was
collected by boat from the lee side of Heron reef and from the entrance of One Tree
reef. Although Heron reef water (12 km away) could not be collected every day,
special care was taken to ensure that the age of the water being used in the flume tests
was the same for One Tree and Heron water. Water was never held in buckets for
longer than 2 days. No significant effect of age of water was found either in 2006
(ANOVA: F1,2¼ 1.236, P¼ 0.28) or in 2007 (ANOVA: F1,2¼ 0.9249, P¼ 0.40).The larvae captured on a given day, numbers determined by the ‘‘catch of the
day’’, were held in a glass aquarium with water from One Tree reef until their first
olfactory preference test with One Tree versus Heron reef water. The majority of
initial preference tests were completed within 12 h of capture, but never more than
36 h after capture. Each fish was tested individually and after this initial test
(‘‘day 0’’) was randomly assigned to either the One Tree or Heron acclimation group,
and kept for up to 9 days in aquaria with water either from One Tree or Heron reef.
Aquaria were kept at ambient temperature (�29�C) with an air stone in each tank.
In these tanks, 50% of water was changed every day with fresh Heron or One Tree
water collected on the same or previous day. Each individual fish was tested for their
preference for One Tree or Heron water up to six times, on days 0, 1, 2, 4, 6, and 9 in
2006 and, for logistical reasons, on days 0, 1, 2, 3, and 5 in 2007. All of the fish used
in this experiment were captured at One Tree. We refer to fish that were subsequently
held in One Tree water as One Tree-acclimated and fish held in Heron water as
Heron-acclimated.Preference tests were conducted in our miniflume, a small, two-channel Plexiglas
choice flume 23� 5 cm2 (Gerlach et al. 2007; Munday et al. 2009). The miniflume
maintained two parallel flows siphoned at 100mLmin�1 per channel (monitored
with a Gilson in-line flow meter) from buckets of One Tree or Heron reef water.
Each flow entered the flume through a fine screen collimator. The upstream half of
this flume was separated by a plexiglass divider creating two channels; the
downstream area of the flume was open between the two sides creating a testing
area where fish could move back and forth between water masses and sample both
types of water being presented. Dye tests were performed at the beginning of each
testing session to verify that the two water flows remained separated throughout the
length of the flume with little mixing.In order to test preference for One Tree versus Heron water an individual fish
was removed from its holding tank and placed in the testing area of the flume.
Catching the fish with a small net and placing it in the flume took less than 30 s. If
the fish did not initially swim to each side, it was gently moved between sides so that
it could sense the different odors present. The fish was allowed to acclimate for at
least 1min or until it was swimming or hovering calmly. Each trial lasted 2min
during which the position of the fish’s nose (left or right of the midline) was recorded
every 5 s. After the first 2min trial, the reef odors were switched so that if One Tree
water was originally on the left it was now on the right and vice versa for Heron
water to account for possible side bias of individual fish. After 1min to allow the
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flows to fully re-establish themselves (no fish observations recorded) a second 2min
trial was observed. This resulted in a total of 48 observations over 4min.For each individual fish, we calculated its preference in percent for One Tree
water from the number of times the test fish was observed in One Tree minus the
number of times that it was observed in Heron water. A preference of 0% indicates
that the fish spent an equal amount of time in One Tree and Heron water. A positive
percentage indicates that larvae spent more time in One Tree water and a negative
percentage indicates that larvae spent more time in Heron water. A Wilcoxon signed-
rank test (JMP version 5.1 SAS Institute) was used to determine whether the mean
preference of all the fish acclimated in One Tree or Heron water was different from
zero on a given day. A multivariate analysis of variance (MANOVA) analysis for
repeated measurements was used to determine whether there was a significant effect
of acclimation water and test days using the mean preference of each group. We
could not follow olfactory preference of individuals since logistical demands dictated
that groups of fish captured on the same day were held together in the same tank
(One Tree or Heron).Fish were analyzed in three groups: (1) O. doederleini, (2) pooled other
apogonids, and (3) P. coelestis. A total of 17 O. doederleini were captured in 2006
and 34 in 2007. There were five Heron and six One Tree groups consisting of 1–8
individuals per group. Evaluation by analysis of variance (ANOVA; JMP version 5.1
SAS Institute) showed that results from these 2 years were not different from each
other (ANOVA: year (2006, 2007) F1,5¼ 0.7855, P¼ 0.38), thus, the 2006 and 2007
O. doederleini were pooled for final analysis. A total of 25 O. doederleini were
acclimated in One Tree water and 24 in Heron water. Since time limitations in the
field resulted in different test days between years, we combined days 3/4 and 5/6 and
analyzed water preference for test day 0, day 1, day 2, day 3/4, and day 5/6. A variety
of apogonid larvae were captured in 2006 including three species that could be
identified (C. quinquelineatus, A. properuptus and Pristicon trimaculatus) and four
species of larvae that could not be identified (Apogon sp. 1–4; Table 1). Since the
number of any one species captured was small, these species were pooled together for
analysis to determine whether apogonids in general show a stable preference for the
odor of their settlement reef. A total of 44 apogonids (excluding O. doederleini) were
acclimated in One Tree water and 41 in Heron water. There were 10 One Tree and 9
Heron acclimated groups (each consisting of 1–7 larvae). The number of each species
Table 1. Number of apogonid species in the pooled apogo-nids group acclimated in One Tree and Heron water.
Species One Tree Heron
C. quinquelineatus 19 17A. properuptus 5 5P. trimaculatus 0 1Apogon sp. 1 3 4Apogon sp. 2 11 13Apogon sp. 3 2 2Apogon sp. 4 4 3
Total 44 41
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acclimated in One Tree and Heron water is indicated in Table 1. A total of 20P. coelestis larvae were captured in 2007; 10 were acclimated in One Tree water and10 in Heron water. There were two Heron acclimated and two One Tree acclimatedgroups.
Results
Olfactory preference of O. doederleini
Ostorhinchus doederleini larvae that settled on One Tree reef maintained a significantpreference for One Tree reef water over a period of 2–4 days even when acclimated inHeron water (Figure 1a). There was never a significant difference between One Treeand Heron acclimation groups. On day 0, the fish captured in One Tree lagoonshowed a significant preference for One Tree water (12.1%þ/� 3.5%, Wilcoxonsigned-ranks test: T¼ 262, P5 0.001). On subsequent days, none of the groups,including those acclimated in Heron water, developed a preference for Heron water.There was no significant difference between One Tree and Heron acclimated fish onany day of testing (ANOVA (OTI, H): day 1 F1,47¼ 0.17, P¼ 0.69; day 2 F1,45¼ 0.80,P¼ 0.38; day 3 F1,45¼ 0.85, P¼ 0.85; day 5 F1,33¼ 0.02, P¼ 0.88). A MANOVA forrepeated measurements was performed by using the means of each capture group; forO. doederleini, there were five Heron and six One Tree capture groups consistingof one to eight individuals per group. There was no significant effect of source of
Figure 1. Mean percent preference for One Tree water of all individual larvae tested on agiven day of acclimation. Larvae were collected from One Tree and acclimated in One Treewater (circles, solid trend line) or Heron water (squares, dashed trend line). Error bars showstandard error of the mean. Asterisks denote values that are significantly different from 0(Wilcoxon signed ranks-test). Numbers denote sample size. Negative values (not found) wouldindicate a preference for Heron water. No significant difference was found between Heron andOne Tree acclimated groups on any day. (a) O. doederleini and (b) other apogonids and(c) P. coelestis.
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acclimation water, days of acclimation, or the interaction of both on olfactorypreference (MANOVA: acclimation water (OTI, H) F1,9¼ 0.28, P¼ 0.61; day(0, 1, 2, 3, 5) F4,6¼ 0.06, P¼ 0.99; acclimation water by day F4,6¼ 0.28, P¼ 0.88).A small decline in preference over time was observed under both acclimationconditions. Since the declining trends were similar for One Tree and Heronacclimation groups it reflects an effect of time; there was never a reversal ofpreference. It is therefore illustrative to consider the trend lines: their extrapolationsintercept the zero line (no preference) at 33 and 15 days for One Tree and Heronacclimation, respectively.
Olfactory preference of other apogonids
Like O. doederleini, the treatment consisting of all other apogonids combined did notshow any evidence for changes in preference based on duration of acclimation. Onday 0, the other apogonids, captured in One Tree lagoon showed significantpreference for One Tree water similar to O. doederleini’s preference (11.8% þ/�3.3%, Wilcoxon signed-ranks test: T¼ 473, P5 0.005). Acclimation water did notaffect larval preference for One Tree water (Figure 1b). There was no differencebetween One Tree and Heron acclimated fish on any day (ANOVA (OTI, H): day 1F1,78¼ 1.42, P¼ 0.24; day 2 F1,68¼ 0.14, P¼ 0.71; day 4 F1,60¼ 0.12, P¼ 0.73; day 6F1,46¼ 0.52, P¼ 0.48; day 9 F1,40¼ 0.17, P¼ 0.68). A MANOVA for repeatedmeasurements of 10 One Tree and 9 Heron acclimated capture groups (eachconsisting of 1–7 larvae) demonstrated that neither the source of acclimation waternor days of acclimation nor the interaction of both had an effect on olfactorypreference (MANOVA: acclimation water (OTI, H) F1,16¼ 0.13, P¼ 0.73; day(0, 1, 2, 4, 6, 9) F4,13¼ 0.29, P¼ 0.88; acclimation water by day F4,13¼ 0.53, P¼ 0.72).Despite a non-significant 9-day declining trend in One Tree preference in bothacclimation groups, Heron-acclimated apogonids never developed a preference forHeron water and acclimation had no significant effect on their persistent preferencefor One Tree water. Declining trend lines intercept the zero line at 14 and 21 daysafter the start of acclimation to One Tree and Heron water, respectively.
Olfactory preference of P. coelestis
Settling P. coelestis larvae caught at One Tree showed significant preference for OneTree water and maintained this preference for 1 day regardless of acclimation water;this preference declined quickly both in One Tree and Heron acclimation groups(Figure 1c). On day 0, the larvae showed a significant preference for One Tree water(16.7%þ/� 6.1%, Wilcoxon signed-ranks test: T¼ 45, P5 0.005). Although thisspecies showed a clear decline in preference during the acclimation period, the declinewas again similar in both groups; therefore acclimation odor had no effect onpreference for One Tree water. There was no difference between One Tree and Heronacclimated fish on any day (ANOVA (OTI, H): day 1 F1,18¼ 0.11, P¼ 0.74; day 2F1,18¼ 0.98, P¼ 0.33; day 3 F1,18¼ 0.85, P¼ 0.37; day 5 F1,18¼ 0.12, P¼ 0.73). Byday 5, the preference for One Tree water had declined to zero in both One Tree andHeron acclimated larvae, suggesting again that time in captivity, not acclimationodor, wiped out preference for One Tree water. Heron-acclimation never led to apreference for Heron water. Visual inspection of the data shows loss of odor
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preference as early as days 2 and 3. A repeated measures MANOVA was notperformed for this species because there were only two groups of fish in eachcondition.
Discussion
The results show that at the time of settlement on One Tree, all of the species testedpreferred the odor of One Tree water to Heron water; settlers transferred to Heronwater did not change their preference but rather preferred One Tree water for severaldays. Ostorhinchus doederleini and other cardinal fish maintained their preference fora longer time than P. coelestis. Eventually, both species stopped showing anypreference for One Tree or Heron water either as a response to captivity or becausethe fish settled during the course of the experiment, however, none of the speciestested switched to prefer the new odor.
The question of great interest for understanding recruitment processes is whenand how settling larval reef fish learned their odor preference. For most species ofreef fish, the specific chemical cues used by larvae to recognize reefs are unknown.Each reef may have a unique odor based on the chemical composition of thebiological assemblage that inhabits that reef, including coral species, terrestrialdetritus, conspecifics and even kin (Sweatman 1988; Elliott et al. 1995; Lecchini et al.2005; Doving et al. 2006; Dixson et al. 2008). The milieu of chemical cues used todistinguish between specific reefs within a reef group is likely to be complex leadingto the idea that the preference for the settlement reef is probably learned and notinnate. Since larval reef fishes have a nose at hatching it is possible for them toimprint on the odor of their natal reef at birth (Arvedlund et al. 2000b; Arvedlundet al. 2003). Anemonefish learn the odor of their host sea anemone before leaving thereef in order to recognize and settle on the correct anemone species when they return(Arvedlund and Nielsen 1996; Arvedlund et al. 1999; Arvedlund et al. 2000a) andzebrafish larvae imprint on kin odor on day 6 post-fertilization (Gerlach et al. 2008).Apogonids mouth brood their eggs and pomacentrids defend benthic eggs. Bothtypes of larvae are exposed to conspecific, kin and reef odor throughout the egg stageand immediately after hatching and could imprint on these odors during this time.
Reef fish could also learn the birth reef odor later: at the developmental stagewhen reef currents transport them out of the reef they can hardly swim. This keepsthem passively entrained in the reef current and exposed to its odor for several daysuntil their water mass becomes fully mixed with other water through the eddycascade (Kolomogorov scale; Atema et al. 2002). This would give them time forfurther olfactory development and imprinting. By the time the larvae developswimming capabilities they can then begin to use their odor preference to maintaincontact with the odor halo of their birth reef. Unfortunately, pre-settlement larvaeare hard to find and even harder to test so we cannot draw the previous scenario toconclusion.
The alternate interpretation is that the reef fish species test learned the odor ofthe settlement reef on the day they were caught. If that were so, we would expectthem to switch that odor preference as fast as they had learned it. Based on theresults, we reject this hypothesis. So a possible explanation is that they learned thesettlement reef odor in the last several days before settling. This would suggest thatthey allow themselves to be dispersed without reef odor knowledge for the majority
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of the pelagic larval period, end up somewhere, perhaps near a reef, and then learnthe odor of that environment. This would then enhance their ability to remain nearthe newfound reef. Until we can test presettlement larvae we cannot draw firmconclusions. Olfactory preference for the settlement reef, whether learned at birth orlater, would increase settlement success and recruitment to the reef.
Acknowledgements
We thank M. O’Callaghan and F. Smith for assistance with sample collection. This study wasfunded by the National Science Foundation OCE-0452885 to Gabriele Gerlach and JelleAtema, National Geographic Society, Grant no. 7236-02, ARC grants and funding from theARC Centre of Excellence for Coral Reef Studies to Michael Kingsford and, a NationalScience Foundation Graduate Research Fellowship to Vanessa Miller-Sims.
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