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A Highly Social, Landdwelling Fish Defends Territories in a Constantly

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A Highly Social, Landdwelling Fish Defends Territories in a Constantly Ethology A Highly Social, Land-Dwelling Fish Defends Territories in a Constantly Fluctuating Environment Terry J. Ord* & S. Tonia Hsieh * Evolution and Ecology Research Centre, and the School of Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, NSW, Australia Department of Biology, Temple University, Philadelphia, PA, USA Correspondence Abstract Terry J. Ord, Evolution and Ecology Research Centre, and the School of Biological, Earth The Pacific leaping blenny (Alticus arnoldorum) is a marine fish that has and Environmental Sciences, University of made a highly successful transition to land. We report an extensive field New South Wales, Kensington, 2052 NSW, study on the behavior of this remarkable fish and how it has coped with Australia. life on land. The fish occurs in great abundance above the waterline E-mail: [email protected] along the rocky coastlines of Micronesia. We found them to be terres- trial in all aspects of their adult daily life, but heavily constrained by S. Tonia Hsieh, Department of Biology, Temple University, Philadelphia, PA, 19122, large fluctuations in both tide and temperature with almost all activity USA. limited to a brief period at mid-tide. Despite this, the fish were highly E-mail: [email protected] social and data were consistent with males defending exclusive territo- ries on land. A variety of metrics – the use of visual displays, the allom- Received: July 21, 2011 etry of ornaments, and sexual dimorphism – further imply sexual Initial acceptance: July 25, 2011 selection on both sexes was strong. Despite being restricted to an extre- Final acceptance: July 25, 2011 mely narrow habitable zone in which conditions change constantly, the (M. Herberstein) Pacific leaping blenny is remarkably adapted to life on land and rarely doi: 10.1111/j.1439-0310.2011.01949.x returned to water. The genus is unique among the living fishes in its degree of terrestriality and serves as a useful model of the constraints and adaptations that accompany major ecological transitions. 2009). A unique opportunity to examine the conse- Introduction quences of a water–land transition on behavior is The invasion of land by fish in the late Devonian offered by a number of contemporary examples was a critical step in vertebrate evolution. How these where fish have made a similar transition onto land early fish adapted physiologically and morphologi- (Sayer & Davenport 1991; Martin 1995; Sayer cally to the dramatic change in environment associ- 2005). While these present-day fishes differ in ated with the transition to land can be partly important ways from the first colonizers of land in inferred from fossils (e.g., Coates & Clack 1990; the Devonian, they are useful living examples of the Daeschler et al. 2006; Long et al. 2006). Yet, the ways in which land colonization can be achieved selective pressures experienced in a terrestrial envi- from an aquatic origin. ronment by an animal that, at least initially, retained The comb-toothed blennies (family Blenniidae) much of its ancestral aquatic phenotype are difficult consist of slender, elongate-bodied fishes that are to appreciate from fossils alone. Of particular rele- ancestrally aquatic and benthic in habit (Patzner vance is behavior, because the way in which animals et al. 2009). However, there are several species interact with one another and the environment of blenny that are noteworthy because of their determines the nature of selection experienced by frequent terrestrial activity on rocks in the intertidal species. Obtaining behavioral information on extinct zone (Sayer & Davenport 1991; Martin 1995; species is generally limited to extrapolation from the Hsieh 2010). Previous observations on some of these fossil record (e.g., Varricchio et al. 2008; Mazin et al. species suggest that they seldom, if ever, voluntarily 918 Ethology 117 (2011) 918–927 ª 2011 Blackwell Verlag GmbH T. J. Ord & S. T. Hsieh Behavior of a Land-Dwelling Fish submerge themselves underwater and can stay indef- side of Guam during what we anticipated would be initely on land if they remain moist (Brown et al. the start of the breeding season (April; see Shimizu 1991; Bhikajee & Green 2002; Hsieh 2010). Surpris- et al. 2006). The first site was approx. 500 m north ingly, despite their high abundance at localities of Talofofo Bay at a small cove immediately adjacent throughout the tropical Pacific, very little is known to route 4. Here, Pacific leaping blennies were found about the behavioral ecology of these remarkable in high abundance along a 600-m stretch of open land-dwelling fishes. Here, we report the first behav- rocky shoreline that could be accessed by bush trails ioral study of the Pacific leaping blenny, Alticus ar- or from the water by wading along the reef. The sec- noldorum. While amphibious behavior seems quite ond site was 300 m north of Tagachang Beach and common in fish generally (Sayer & Davenport 1991; was only accessible by wading through the surf. At Martin 1995; Martin et al. 2004; Sayer 2005), the this site, blennies were found in high abundance Pacific leaping blenny is one of the rare living exam- along a 500-m stretch of rocky outcrops under the ples of a fish that spends the vast majority of its time cliffs. The two sites were roughly 10 km apart and on land. Our aim was to determine the consequences separated by multiple beaches and other terrestrial of a terrestrial lifestyle on the behavioral ecology of barriers. We refer to blennies at each location as this fish, which has apparently made a highly suc- belonging to the Talofofo and Tagachang popula- cessful transition cross the water–land interface. tions, respectively. The Pacific leaping blenny is a small marine fish We established six transects at each location and (4–8 cm in length) that occurs in high densities counted the number of adults, irrespective of sex, at along the rocky coastline of Guam (Fig. S1). The fish hourly intervals over a single day between 0930 and are extremely agile on land, moving quickly over 1830 hrs (Talofofo: 3 April, 2009; Tagachang: 4 complex rocky surfaces using a unique tail-twisting April, 2009). We chose intervals of an hour to mini- behavior combined with expanded pectoral and tail mize the effect of any disturbance to fish in consecu- fin morphology that allows them to adhere to almost tive consensus periods. It is important to note that, any firm surface (Hsieh 2010). Nevertheless, life on while transects varied in length (20–90 m), our land still comes with severe constraints for these objective was to document changes in abundance fish. Like other marine amphibious fishes, blennies within transects over time and not to compare densi- do not possess an air-breathing organ (lung), but ties among transects and populations. rely on the exchange of O2 and CO2 through the skin and gills when on land (Martin & Lighton 1989; Behavioral Observations Brown et al. 1992). Terrestrial blennies must conse- quently remain moist to avoid asphyxiation. This Following abundance surveys, we conducted detail restricts these fish to the wet intertidal rocks within behavioral observations on individual adult males the splash zone. With this in mind, we began our and females. For each population, observations were field study by first determining how the extremes in conducted on consecutive days between 0730 and tide level and air temperature impacted the activity 1730 h with a median interval between observations of the Pacific leaping blenny. We then conducted a of 30 min (Talofofo: 6–11 April, 2009; Tagachang: detailed investigation into the social behavior of 13–19 April, 2009). Observations consisted of 15- adults and found that intrasexual and intersexual min focal sampling in which we verbally recorded interactions were frequent and mediated by conspic- all behavior performed by the subject on a water- uous visual signals in both sexes. Finally, we proofed microcassette recorder. During this period, attempted to identify the cues encoded in a set of we also performed scan samples at 1-min intervals these visual signals; in particular, the color and to note the number of males, females, and subadults allometry of the brightly colored dorsal fin ‘flashed’ (sex unknown) within 20 cm of the subject. At the during aggressive disputes by both sexes, as well as a end of observations, we attempted to catch the sub- prominent fleshy head crest possessed by males. ject for morphological measurements and color photography (see ‘Morphological Measurements’ below). Our catch rate was modest (approx. 63%), Methods reflecting the agility of these fish on land and ability to evade capture by even the most determined Adult Abundance researcher. We began our study by conducting a general survey Audiotape recordings were scored by a single lis- of adult numbers at two locations on the eastern tener (TJO) using JWATCHER ver 1.0 event recorder Ethology 117 (2011) 918–927 ª 2011 Blackwell Verlag GmbH 919 Behavior of a Land-Dwelling Fish T. J. Ord & S. T. Hsieh software (Blumstein & Daniel 2007). A total of ered all realistic combinations of predictor variables 61 males and 71 females were sampled at Talofofo and weighed the evidence for each model simulta- (33 h of observation), while 66 males and 61 neously. Abundance was assessed as the number of females were sampled at Tagachang (32 h of obser- adults of either sex recorded at hourly intervals vation). during transect surveys (see ‘Adult Abundance’). Activity data consisted of three behaviors that were among the most common during the 15-min Morphological Measurements focal samples. Those behaviors were as follows: Those individuals caught at the end of our observa- total time spent moving about on rocks, total time tions were weighed using an Ohaus digital balance spent feeding off algae on rocks, and total number (Model CS200, Ohaus Corporation, Pine Brook, NJ, of aggressive interactions defined as either displac- USA) to the nearest 0.1 g.
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