Marine Biology (2018) 165:184 https://doi.org/10.1007/s00227-018-3444-6

ORIGINAL PAPER

Nest building by a small mesograzer limits blade size of the giant kelp Macrocystis pyrifera

Alistair G. B. Poore1 · Lars Gutow2 · Anne‑Nina Lörz3 · Martin Thiel4,5,6

Received: 6 February 2018 / Accepted: 8 November 2018 / Published online: 14 November 2018 © Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract Small herbivores are abundant on large marine macrophytes, but their impact on their hosts is poorly understood relative to large grazers such as urchins and fsh. To limit the risks of predation, many marine mesograzers live within nests or bur- rows, potentially causing more damage to plants than predicted from consumption alone. To test whether the growth of large primary producers can be afected by modifcation of plant structures by small herbivores, we quantifed the efect of the nest-building amphipod Pseudopleonexes lessoniae on blades of the giant kelp, Macrocystis pyrifera in New Zealand. Amphipods create their nests by rolling the blade margin in close proximity to the meristem. Blades with nests were 40% shorter than blades lacking nests and reduced in area by 55%. We examined the composition of amphipods inhabiting each nest to assess the temporal persistence of grazer aggregations. Nests were occupied by a single female or male–female pairs, and their newly hatched ofspring. Analysis of ofspring size distributions suggested that ofspring dispersed from the maternal nest and did not remain to breed themselves. By concentrating physical damage and feeding on valuable tissues, these results indicate that even low numbers of small herbivores can cause localized impacts on the morphology and size of fast-growing algal blades. Predicting the consequences of this damage on larger scales will require understanding the spatial and temporal distribution of amphipod nests on giant kelp.

Introduction Responsible Editor: P. Gagnon.

Reviewed by S. Hamilton and an undisclosed expert. Strong impacts of small invertebrate herbivores on the plants they consume are most evident when herbivore populations Electronic supplementary material The online version of this are high, such as during pest outbreaks in agricultural and article (https​://doi.org/10.1007/s0022​7-018-3444-6) contains supplementary material, which is available to authorized users. natural systems (Kozlov and Zvereva 2017). Even at low abundances, however, small herbivores can greatly reduce * Alistair G. B. Poore the performance of individual plants if their feeding activi- [email protected] ties are concentrated on highly valuable plant tissues. Small 1 Evolution and Ecology Research Centre, School herbivores are usually unevenly distributed among plant of Biological, Earth and Environmental Sciences, University parts, and preferential feeding on meristematic, reproduc- of New South Wales, Sydney, NSW 2052, Australia tive or photosynthetically active tissues can lead to impacts 2 Alfred Wegener Institute Helmholtz Centre for Polar on plant ftness that are not easily predicted from the low and Marine Research, Box 120161, 27515 Bremerhaven, levels of biomass removed by grazing (Doak 1992; Poore Germany et al. 2014). Small amounts of tissue loss can further lead to 3 CeNak, Zoological Institute and Museum, University an increased risk of structural damage (Marquis 1996) and of Hamburg, Martin‑Luther‑King Platz 3, 20146 Hamburg, access to pathogens (Stout et al. 2006), or facilitate grazing Germany by other species (Molis et al. 2010). 4 Facultad de Ciencias del Mar, Universidad Católica del Damage by small herbivores can also be concentrated on Norte, Larrondo 1281, Coquimbo, Chile specifc plant parts if they aggregate to avoid predators or 5 Millennium Nucleus Ecology and Sustainable Management stressful abiotic conditions, for increased mating opportu- of Oceanic Island (ESMOI), Coquimbo, Chile nities, or as a function of their reproductive biology (e.g., 6 Centro de Estudios Avanzados en Zonas Áridas (CEAZA), sociality, parental care, and limited dispersal of ofspring Larrondo 1281, Coquimbo, Chile

Vol.:(0123456789)1 3 184 Page 2 of 9 Marine Biology (2018) 165:184 after hatching, Thiel 2003). Many small herbivores inhabit species for the genus Pseudopleonexes (Conlan 1982). The modifed plant structures that ofer protection (e.g., burrows species is a common inhabitant of M. pyrifera in the Wel- within leaves and stems, galls or rolled leaves, Lill and Mar- lington area and has been observed to damage individual quis 2007). Given that these structures concentrate tissue blades (Pérez-Matus and Shima 2010). Initial observations damage on specifc plant parts, understanding the place- (M. Thiel) suggested that P. lessoniae often builds nests at ment of the structures relative to the value of these tissues, the base of the blade, in contrast to other species from this and their persistence in time, is needed to predict the likely family that prefer to build nests at the distal tips of the fronds impacts of this behaviour on plant ftness. of M. pyrifera (Cerda et al. 2010). Any concentration of To test the potential of structures created by small herbi- grazing damage to the meristematic region at the base of the vores to impact large primary producers, we examined the blade has the potential for greater impacts on growth of that efect of a nest-building amphipod on blades of the giant blade than widely distributed damage, or damage to older kelp, Macrocystis pyrifera. Kelps and other macroalgae are tissue. Additionally, larger nests likely have greater impacts dominant habitat-forming organisms in temperate marine on the growth of individual blades than smaller nests as they ecosystems worldwide and support a diverse community of may disturb larger areas of sensitive tissue. To test these associated organisms (Schiel and Foster 2015). High densi- hypotheses, we quantifed the size and location of nests rela- ties of mesograzers, including isopods, amphipods, small tive to valuable meristematic tissue within individual kelp gastropods, frequently inhabit kelp canopies, but there is blades. By contrasting nest blades with similarly aged blades limited evidence to date for strong impacts on kelp growth without nests, we tested how the size and morphology of and survivorship in contrast to the well-known impacts of kelp blades are altered by the presence of amphipod nests. large invertebrate grazers such as urchins (Poore et al. 2012). Finally, we determined the composition and size structure Negative impacts by mesograzers on large macroalgae have of amphipods within each nest to describe their reproductive been observed during outbreaks (Chess 1993; Graham 2002; biology and to assess the temporal persistence of grazing Pfster and Betcher 2018), in mesocosm experiments (Dufy damage on individual blades. If nests are sites of reproduc- and Hay 2000), and in some feld experiments (Davenport tion and there is evidence for limited dispersal of ofspring and Anderson 2007; Poore et al. 2014). from the maternal environment, then we would expect that Like insects on terrestrial plants, some marine crusta- grazing damage is concentrated in comparison to short-lived cean mesograzers modify plant structures to create nests, nests with ofspring rapidly dispersing from the maternal tubes and burrows (Mejaes et al. 2015; Moore and Eastman environment. 2015). Among the most abundant mesograzers in vegetated marine substrata are amphipods from the family Ampithoi- dae, with approximately 230 species, belonging to 15 genera Materials and methods (Poore et al. 2008; Horton et al. 2017). Species from this family form silken tubes on algal surfaces (Appadoo and Sampling of kelp blades and amphipods Myers 2002), burrow into kelp stipes (Chess 1993) or fold algal blades into tubes or nests, often termed “kelp curl- Macrocystis pyrifera and amphipods were collected from ers” (Graham 2002; Cerda et al. 2010). Burrows and nests Breakers Bay, Wellington, New Zealand (41°19’55.0”S, are frequently sites of reproduction and can house multiple 174°49’53.5”E) on three consecutive days during austral cohorts of ofspring derived from the individuals that ini- summer 2012/13 (30 January to 1 February 2013). Sampling tially constructed the domicile (Conlan and Chess 1992). was done by snorkeling within a kelp forest at an approxi- While most mesograzers are highly mobile (Taylor 1998; mate water depth of 0.5–1 m, i.e., within the upper sections Poore 2005), those species that reside and reproduce within of the kelp canopy. At the site, kelps grow at water depths burrows or nests are likely to concentrate their feeding dam- of 3–10 m. age on particular parts of the plant and could impact plant In the feld, we examined the upper parts of the kelps, growth more strongly than those herbivores whose grazing searching for blades with nests. We searched from the apical damage is widely distributed among plant parts. meristem downwards until we encountered the frst blade Here, we examined the localized effects of the nest- with an amphipod nest. Nests were easily found, and we esti- building amphipod Pseudopleonexes lessoniae (Hurley mated that more than 50% of stipes had blades with nests. 1954) (Ampithoidae) on the growth and morphology of Once a nest was identifed on a stipe, we cut the stipe below M. pyrifera blades in a kelp forest in New Zealand. The that blade and above the adjacent upper blade, placing the Ampithoidae are represented by four genera in New Zealand stipe segment with the two blades carefully in a Ziploc bag. waters comprising seven species (Peart and Lörz 2018). This By collecting two blades immediately adjacent to each other, species was originally described by Hurley (1954) as Pleo- one blade with a nest and the one immediately above it with- nexes lessoniae and was subsequently designated the type out a nest, we were able to collect blades of very similar age

1 3 Marine Biology (2018) 165:184 Page 3 of 9 184 from the same kelp individual. We matched the nest blade larger surface area in the undamaged blade) would be asso- with the adjacent upper blade, which is closer to the growth ciated with greater tissue loss in the blade with a nest than meristem of the stipe and therefore slightly younger than the younger pairs of blades. To test this hypothesis, we used lin- nest blade. Sixty-two pairs of blades were sampled with fve ear regression to contrast the loss of tissue assumed to result of these excluded from analyses when the blade thought to from the presence of the nest (i.e., length of blade lacking be lacking a nest was found to have a nest present. nest—length of adjacent blade with nest) to the length of the The amphipods typically remained in their nests when blades lacking nests. A similar analysis was then conducted blades were placed into the Ziploc bags, and thus we are for loss of surface area. confdent that no inhabitants of a nest were lost during sam- To test whether larger nests, or those closer to the mer- pling. In fact, many amphipods were still inside their nests istem, were associated with greater reductions in blade several hours after feld sampling when the samples were growth, we used linear regression to contrast the assumed processed in the laboratory. Samples were transferred back loss in length to nest position (distance from the meristem to the lab alive within 1 h after sampling. In the lab, all to the edge of the nest closest to the meristem) and nest size amphipods were carefully removed from the nest, and the (length of nest along blade margin) (separate analyses for kelp blades and Ziploc bags were carefully scanned for any each independent variable). The loss in length and area of amphipods that had abandoned their nests during sampling, individual blades were contrasted in separate linear regres- transport and processing. All amphipods were preserved in sions to the total number of amphipods, and the number of 70% ethanol. In a few cases, single blades supported more adults per nest to test whether the abundance of amphipods than one nest, and in these cases, amphipods were collected in each nest could predict damage to individual blades of M. from the largest nest. pyrifera. All analyses were conducted in R version 3.4.1 (R The amphipod material of P. lessoniae is held at the Core Team 2017). National Institute of Water and Atmospheric Research (NIWA) Invertebrate collection (registration numbers NIWA Composition of amphipods within nests 96675–96677, NIWA 96688–96698, NIWA 96797–96804, NIWA 96810–96818 and others from the same collection Of the 57 pairs of blades examined, 48 harboured P. les- site). soniae in the nests at the time of sampling. Amphipod specimens were examined using a Leica MZ12.5 dissect- Efects of nests on blades ing microscope and identifed to species, with 283 of 285 individuals collected (99%) identifed as P. lessoniae. Male The efect of nest building by P. lessoniae on M. pyrifera P. lessoniae were identifed based on their comparatively blades was determined by contrasting the size of blades large 2nd gnathopod and females were determined based on with nests to the directly adjacent blade that lacked a nest. the presence of the marsupium and the less setose 2nd gna- The total length of each kelp blade was measured from the thopod (Hurley 1954). Individuals that could not be sexed base of the blade (where it connects to the pneumatocyst) to were classifed as juveniles. All amphipods were measured the distal-most tip of the blade. The pneumatocyst length, from images taken using a camera connected to the dissect- blade surface area and maximum width of blades were ing microscope, with total length defned as the dorsal line determined from digital images using the image analysis from the anterior part of the head (base of the 1st antenna) software ImageJ (available at https://image​ j.nih.gov/ij/downl​ ​ to the base of the telson. The number of eggs in the mar- oad.html). The position of each nest along the blade, and supia of ovigerous females was counted. We quantifed the nest size were quantifed by recording the distance from the co-occurrence of the sexes, and examined the size structure base of the blade to the beginning and end of the nest. The of juveniles, females and males within each nest, to identify total length, maximum width and surface area of blades with cohorts of ofspring and test whether nests were occupied nests were contrasted to their adjacent blades with paired t by multiple generations. tests. For undamaged blades lacking nests, the length of the pneumatocyst was correlated with the length of the blades Results (t = 5.6, P < 0.001, R2 = 0.33, n = 60). Consequently, to confrm that the blades in each pair were of a similar age, we Efects of nests on Macrocystis pyrifera blades contrasted pneumatocyst lengths within each pair and found no evidence for diferences in length (paired t test, t = 1.1, The nests of P. lessoniae on M. pyrifera are constructed df = 59, P = 0.29). by individual amphipods folding the edge of a blade and If nests were initiated early in the life of each blade, we attaching the folded edge to the remaining blade with silk would expect that older pairs of blades (i.e., longer and with (Fig. 1a) produced by glands at the base of their 3rd and

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Fig. 1 Typical structure of a P. lessoniae nest on the margin of a M. pyrifera blade adjacent to the meristem (a) with the lines marking the proximal and distal edges of the nest used to calculate nest size. The amphi- pod image, modifed from Peart and Lörz (2018), illustrates the size of an adult relative to the nest. Examples of damage to blades with P. lessoniae nests (b). Images are four pairs of adjacent blades from diferent kelp individuals, with amphipod nests present on the blade on the right in each pair

4th pereopods. The nests were, on average (± SE) 68.5 ± 57). There was a similar pattern for blade surface area (t = 4.5 mm long and generally positioned very close to the mer- 8.19, P <0.001, N = 57), with both results supporting the istematic region on each blade, where the base of the blade hypotheses that nests are initiated early in the life of a blade, meets the pneumatocyst. The proximal edge of the nest was and that older blades would have sustained more damage. on average only 29 ± 3.9 mm from the base on blades which Loss in length and area was uncorrelated with the size of the averaged 211.9 ± 17.8 mm in length (Fig. 2a, b). Amphi- nest (length, t = 1.339, P = 0.19; area, t = 0.19, P = 0.85, pod grazing was mostly limited to the nest or its immediate N = 57) and the distance from the start of the nest to the vicinity (i.e., within the folded over blade sections). base of the blade (meristematic region) (Fig. S1, length, t Blades with nests were strikingly diferent in shape from = 0.22, P = 0.83; area, t = 0.29, P = 0.77, N = 57). Neither adjacent blades of very similar age that lacked a nest, often loss in length nor area was correlated with the total number with a curved rather than straight morphology (Fig. 1b). The of individual amphipods within the nest (length, t = 0.41, P blades with nests were, on average, 40 ± 4.3% shorter and = 0.68; area, t = 1.22, P = 0.0.23, N = 42). had a surface area 55 ± 4.6% smaller than adjacent blades lacking a nest (Fig. 2b, length, paired t tests, t = 8.34, df = Composition of amphipods within nests 59, P < 0.001; Fig. 2c, area, t = 7.53, df = 59, P < 0.001). The loss in length, assumed to result from the presence A total of 283 individuals were collected from the 48 nests of the nest, was positively correlated with the length of the that harboured P. lessoniae at the time of sampling. The sex undamaged blade within each pair (t = 3.8, P < 0.001, N = ratio of adults was female-biased (1.94 female: 1 male, χ2

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Fig. 2 Position of nests relative (a) (b) (c) to the meristem (a), and length 600 600 (b) and surface area (c) of pairs of M. pyrifera blades where one blade contained a nest of P. 500 500 ) lessoniae and the adjacent blade 2 4 n 10 lacked an amphipod nest. ( = 400 400 57 pairs). Note that the y axis in c is on a ­log10 scale Area (mm 300 Length (mm) 300

103 200 200 Distance from meristem (mm)

100 100

102 0 0 Proximal Distal Blade without Blade with Blade without Blade with edge edge nest nest nest nest

= 5.12, df = 1, P = 0.02). The nests were predominantly expected by tissue loss alone. The nests were occupied by occupied by a single adult female (69% of nests) and there individual females, male–female pairs and cohorts of their was never more than one adult female in each nest. One third newly hatched ofspring. Analysis of size frequency distribu- of nests with females were accompanied by a single male, tions suggest that ofspring disperse from the maternal nest with only one nest having two males present. When adults before reaching maturity. were present, 60% of the nests also harboured juveniles and 21% of the nests had only juveniles present. Mesograzer’s impact on kelps The size distribution of P. lessoniae within the nests indicated three distinct cohorts of juveniles below 4 mm The construction of a small nest by P. lessoniae resulted in (Fig. 3a). These likely correspond to the frst three moults M. pyrifera blades with a changed morphology, and reduced of juveniles following hatching (Fig. 3a). Ovigerous females length (by 40%, on average) and surface area (by 55%, on had an average (± SE) of 19.8 ± 0.7 eggs in their marsu- average) relative to ungrazed blades. Here, a low number pium and the numbers of juveniles in each cohort declined of small amphipods (~ 8–12 mm in length as adults) with sharply with age (1st and youngest: 11.4 ± 2.8; 2nd: 8.2 ± correspondingly low per capita grazing rates was able to 2.3; 3rd and oldest: 3.9 ± 1.5) indicative of either dispersal substantially reduce the size of large kelp blades (on aver- from the nest or mortality. There were no distinct cohorts of age 35 cm long) due to the concentration of feeding and juveniles approaching the size of adults. Some of the females physical damage to the meristematic region on each blade. that were currently ovigerous co-existed with juveniles in With most nests having only adults, the observed damage the second or third cohort (Fig. 3b), indicating that females may be the result of nest building by the individual female produce subsequent broods. When nests had juveniles of the that likely initiated each nest. Our fndings contrast with the smallest cohort, females were never ovigerous, and there was expectation that meristems will be less preferred than older no evidence for multiple cohorts of juveniles within each tissues due to the higher allocation of defensive phlorotan- nest (Fig. 3b). The absence of more than one mature female nins to meristems in many kelps (Cronin 2001), and to the per nest, and the size distribution of individual P. lessoniae experimental studies that describe highest consumption rates within nests, suggests that the ofspring from each female on non-meristematic tissues (e.g., Johnson and Mann 1986; disperse before themselves breeding within that nest. Cerda et al. 2009; Molis et al. 2010). Given that the amphi- pods fold the blade margin to create the nest, the position of the nests could relate to toughness (lower in new tissue) Discussion rather than food quality. Excluding rare outbreaks, most mesograzers consume Blades of the giant kelp Macrocystis pyrifera with nests only a very low proportion of available macrophyte tissues. of the amphipod Pseudopleonexes lessoniae were greatly The potential for mesograzers to impact their hosts, however, reduced in size in contrast to blades lacking nests. Physical is dependent on the spatial distribution of grazing damage. damage and consumption of meristematic tissue led to larger Disproportionate efects on algal growth or survival due reductions in the growth of individual blades than would be to small tissue losses are also expected when grazers feed

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Fig. 3 The size distribution of (a) Size distribution all amphipods (a), and the com- 25 position of females, ovigerous Stage and sex females, males and juveniles 20 within 48 individual nests of P. juvenile

Count 15 lessoniae on M. pyrifera (b). female Vertical lines in b indicate the 10 male approximate size range of each cohort of juveniles in a 5 0 (b) Composition

Stage and sex 40 egg juvenile female male 30 Nest

20

10

0 02468101214 Length (mm)

preferentially on reproductive tissues (e.g., the amphipod harbours extensive bacterial colonies on pits along its exo- Parhyalella penai consuming Lessonia nigrescens, Pansch skeleton (Peart and Lörz 2018) but their functional role is et al. 2008, the gastropod Lacuna vincta feeding on Saccha- unknown. rina latissima, O’Brien and Scheibling 2016) or photosyn- The blades of M. pyrifera are the primary sites of photo- thetically active tissue (e.g., Amphoroidea typa consuming synthesis (Arnold and Manley 1986; Zimmerman and Kre- Lessonia spicata, Poore et al. 2014). Small amounts of tissue mer 1986), and loss of blade area is expected to negatively loss can also result in further structural damage (e.g., los- impact kelp individuals. Predicting the impacts of blade loss ing entire kelp fronds to wave action following grazer dam- or reduced blade size on individuals in this population will age, Muñoz and Santelices 1989; Krumhansl et al. 2011), require feld data on the abundance and distribution of nests facilitate feeding by other grazers (Molis et al. 2010), induce among blades within stipes at varying distance from the higher levels of chemical defence that could alter feeding seafoor, as done for Sunamphitoe femorata on M. pyrifera rates of other herbivores (Toth and Pavia 2007), or enhance in Chile, Gutow et al. 2012), and longer-term experiments the spread of disease (Campbell et al. 2014). While P. les- to establish the relationship between photosynthetic area soniae and most other ampithoid amphipods consume algal and likely reproductive output. Fecundity of M. pyrifera is material within their nests (Poore et al. 2008), it is not pos- expected to decline with reducing vegetative biomass due sible from feld sampling alone to determine how much of to lower levels of carbon translocated to sporophylls (Reed the observed efects on blade size are due to grazing only or 1987). Estimating impacts at scales beyond the kelp indi- additional physical damage incurred during nest building. vidual will require data on the spatial and temporal vari- Localized impacts could be further enhanced by bacterial ation in amphipod abundance in the kelp forest. Pseudo- infection of damaged tissue. Pseudopleonexes lessoniae pleonexes lessoniae occurs at the study site at densities of

1 3 Marine Biology (2018) 165:184 Page 7 of 9 184 approximately 12 individuals per frond (Pérez-Matus and behaviour of Sunamphitoe femorata on M. pyrifera blades in Shima 2010), but the seasonality of grazing is currently the kelp forests of Chile. That species also gains protection unknown, and higher impacts are possible during periods from fsh by living within a nest formed by rolling blades, of lower kelp growth. In mesocosm experiments, blades but nests occur almost exclusively in the distal section of of M. pyrifera that had been grazed by P. lessoniae com- blades, far removed from the meristem (Gutow et al. 2012). monly became detached from the pneumatocyst within 3 As blades rapidly grow from the basal meristem, amphipods days (Pérez-Matus and Shima 2010). advance their nests at similar rates (~ 10 mm day−1) toward While our fndings are limited to describing localized the meristem (Cerda et al. 2010). Their grazing damages damage, our results contribute to the growing body of lit- nest walls, but the continuous advancement of nests towards erature that demonstrates the potential for small crustacean younger, undamaged tissue allows for persistence of the nest mesograzers to damage large kelps under certain conditions. despite distal loss of damaged blade tissue. With the meris- Extensive damage to M. pyrifera in California has been tem undamaged, blade elongation rates can efectively com- observed during outbreaks of another ampithoid amphipod, pensate for damage due to amphipod grazing (Cerda et al. the kelp curler Sunamphitoe humeralis, in El Niño condi- 2009). Other kelp-curling amphipods also build nests on tions that were associated with unusually low abundances the distal tips of blades (S. humeralis on M. pyrifera, Jones of predatory fsh (Tegner and Dayton 1987; Graham 2002). 1971; S. africana on Ecklonia maxima, Grifths 1979). In Field experiments in the same system had shown that amphi- contrast to these species, the positioning of the nests by P. pod grazing can result in kelp individuals producing fewer lessoniae close to the meristem likely compromises the long- fronds and meristems (Davenport and Anderson 2007). The term persistence of the protective nest. The diference in closely related Sunamphitoe stypotrupetes burrows into the size between similarly aged blades with and without nests stipes of Laminaria setchellii in California, with outbreaks was higher for pairs of blades assumed to be older. This resulting in the death of kelps from within an entire bed suggests that nests are initiated early in blade development (Chess 1993). On long time scales, amphipod infestation and we predict that the degradation of the surrounding tis- of stipes is positively associated with mortality of the kelp sues (Fig. 1b) would eventually promote the dispersal of Pleurophycus gardneri in Washington (Pfster and Betcher both ofspring and adults to form nests on new blades. In S. 2018). In kelp forests of Chile, fronds of Lessonia spicata femorata, most females changed nests on M. pyrifera within and M. pyrifera are frequently damaged by the isopod A. a 14 day experiment (Cerda et al. 2010). Among leaf-tying typa, with the damage limiting blade growth of L. spicata, caterpillars on land, food limitation promotes dispersal but not M. pyrifera (Poore et al. 2014). despite the increased risk of predation associated with leav- ing protective structures (Sliwinski and Sigmon 2013). Structure and function of amphipod nests The scarcity of older juveniles within the nests, and the observation that nests never harboured more than one female Small herbivores living on both marine and terrestrial plants or male–female pair, indicates that ofspring disperse from commonly mitigate predation risk by modifying plant struc- the maternal environment before attaining maturity. The tures and living within burrows, galls or rolled leaves (Lill nests of P. lessoniae on M. pyrifera were mostly occupied and Marquis 2007; Gutow et al. 2012). Pérez-Matus and by a single female and their juvenile ofspring, with a third Shima (2010) demonstrated that P. lessoniae is vulnerable of these females being accompanied by a single mature to predation by the wrasse Notolabrus celidotus in M. pyrif- male. Three size cohorts of ofspring were evident, corre- era forests in Wellington, and that predation by this and a sponding to the frst few moults after hatching. The levels second species, N. fucicola, indirectly reduces grazing dam- of maternal care in P. lessoniae are like those seen in other age to kelp due to altered amphipod behaviour. While the species of this family, with nests of Exampithoe kutti on the presence of fsh reduced overall grazing damage, it is also brown alga Dictyopteris acrostichoides featuring a single likely to result in damage being concentrated in areas close adult or pair with one brood of ofspring (Poore and Lowry to protective structures. Small herbivores frequently display 1997), and tubes of Cymadusa flosa frequently shared by a aggregated spatial distributions (e.g., gastropods, Johnson male–female pair (Appadoo and Myers 2002). There was no and Mann 1986, and isopods, Poore et al. 2014, on kelps), evidence for the longer-term coexistence of juveniles within and the impact of this on plant ftness will depend on both the nest, as is seen for S. stypotrupetes, where three distinct their location relative to valuable tissues (discussed above), cohorts of ofspring derived from a single male–female pair and how long aggregations persist. Structures that are sites can remain in burrows within Laminaria setchellii until the of repeated reproductive events would further concentrate oldest approach the size of adults (Conlan and Chess 1992; feeding damage and likely impacts on kelp hosts. Chess 1993). The location of nests and impact of P. lessoniae on kelp On terrestrial plants, the rolling of leaves by insects blades contrasts with the well-described nest-building to form protective structures frequently alters habitat

1 3 184 Page 8 of 9 Marine Biology (2018) 165:184 architecture, nutritional quality of plant tissues and can facil- Arnold KE, Manley SL (1986) Carbon allocation in Macrocystis pyrifera itate the abundance of co-occurring species (Fukui 2001; (Phaeophyta): intrinsic variability in photosynthesis Pseudopleonexes lessoniae and respiration. J Phycol 21:154–167 Fukui et al. 2002). clearly alters Bell JE, Bishop MJ, Taylor RB, Williamson JE (2014) Facilita- the morphology of individual blades, but further research tion cascade maintains a kelp community. Mar Ecol Prog Ser is required to test how this localized habitat modifcation 501:1–10 may afect associated epifauna. The burrows, nests and tubes Campbell AH, Vergés A, Steinberg PD (2014) Demographic conse- quences of disease in a habitat-forming seaweed and impacts on of epifaunal invertebrates can be cohabited by other taxa interactions between natural enemies. Ecology 95:142–152 (Mejaes et al. 2015; Moore and Eastman 2015) with these Cerda O, Karsten U, Rothäusler E, Tala F, Thiel M (2009) Compensa- taxa depending on the habitat modifcation. For example, tory growth of the kelp Macrocystis integrifolia (Phaeophyceae, Peramphithoe femorata the canopy-dwelling urchin Holopneustes purpurascens Laminariales) against grazing of (Amphi- Ecklonia radiata poda, Ampithoidae) in northern-central Chile. J Exp Mar Biol rolls fronds of the kelp , creating structures Ecol 377:61–67 that promote the survival of the gastropod Phasianotrochus Cerda O, Hinojosa IA, Thiel M (2010) Nest-building behavior by the eximius (Bell et al. 2014). In contrast, we found only two amphipod Peramphithoe femorata (Krøyer) on the kelp Macro- cystis pyrifera individuals of other animal species inhabiting the nests, sug- (Linnaeus) C. Agardh from northern-central Chile. P. lessoniae Biol Bull 218:248–258 gesting that nests of are unlikely to infuence Chess JR (1993) Efects of the stipe-boring amphipod Peramphithoe other members of the community inhabiting the kelp canopy. stypotrupetes (Corophioidea: Ampithoidae) and grazing gastro- In summary, our study confrms that small marine herbi- pods on the kelp Laminaria setchelli. J Crustac Biol 13:638–646 vores can induce considerable damage to individual blades Conlan KE (1982) Revision of the gammaridean amphipod family Ampithoidae using numerical analytical methods. Can J Zool of a large kelp due to the concentration of feeding and nest- 60:2015–2027 building activities on particularly valuable tissues within Conlan KE, Chess JR (1992) Phylogeny and ecology of a kelp-boring the blade. The loss of blade area resulting from damage to amphipod, Peramphithoe stypotrupetes, new species (Coro- meristematic tissue was clearly disproportional to the low phioidea: Ampithoidae). J Crustac Biol 12:410–442 Cronin G (2001) Resource allocation in seaweeds and marine inverte- per capita grazing rates of tiny amphipods. Predicting the brates: chemical defense patterns in relation to defense theories. impact of small herbivores thus requires data on the spatial In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC distribution of damage, not simply their abundance. Press, Boca Raton, pp 325–353 Davenport AC, Anderson TW (2007) Positive indirect efects of reef Acknowledgements We are very grateful to R. Taylor who hosted MT fshes on kelp performance: the importance of mesograzers. Ecol- during measurements of amphipods at Leigh Marine Lab, and to V. Vil- ogy 88:1548–1561 lalobos for help with image analysis. The NIWA Invertebrate Collec- Doak DF (1992) Lifetime impacts of herbivory for a perennial plant. tion team is thanked for curation of the amphipod material. We thank Ecology 73:2086–2099 P. Gagnon, S. Hamilton and one anonymous reviewer for comments Dufy JE, Hay ME (2000) Strong impacts of grazing amphipods on the that have improved this manuscript. organization of a benthic community. Ecol Monogr 70:237–263 Fukui A (2001) Indirect interactions mediated by leaf shelters in ani- Author contributions mal–plant communities. Popul Ecol 43:31–40 MT conceived the study. MT and AL conducted Fukui A, Murakami M, Konno K, Nakamura M, Ohgushi T (2002) the feld sampling and laboratory measurements. AP analysed the data A leaf-rolling caterpillar improves leaf quality. Entomol Sci and led the writing of the manuscript. 5:263–266 Graham MH (2002) Prolonged reproductive consequences of short- Funding Data evaluation and manuscript writing were done during a term biomass loss in seaweeds. Mar Biol 140:901–911 research stay by LG (fnanced by AWI) and AP (with funding support Grifths CL (1979) A redescription of the kelp curler Ampithoe humer- from FONDECYT Grant 1161383). alis (Crustacea, Amphipoda) from South Africa and its relation- ship to Macropisthopous. Ann S Afr Museum 79:131–138 Compliance with ethical standards Gutow L, Long JD, Cerda O, Hinojosa IA, Rothäusler E, Tala F, Thiel M (2012) Herbivorous amphipods inhabit protective microhabi- Macrocystis pyrifera Conflict of interest tats within thalli of giant kelp . Mar Biol All authors declare that they have no conficts of 159:141–149 interest. Horton T, De Broyer C, Costello M, Bellan-Santini D (2017) Amp- Ethical approval ithoidae Boeck, 1871. In: Horton T, Lowry J, De Broyer C, All applicable international, national, and/or institu- Bellan-Santini D, Coleman CO, Corbari L, Daneliya M, Dauvin tional guidelines for the care and use of animals were followed. J-C, Fišer C, Gasca R, Grabowski M, Guerra-García JM, Hend- rycks E, Hughes L, Jaume D, Jazdzewski K, Kim Y-H, King R, Krapp-Schickel T, LeCroy S, Lörz A-N, Mamos T, Senna AR, Serejo C, Sket B, Souza-Filho JF, Tandberg AH, Thomas J, Thurs- ton M, Vader W, Väinölä R, Vonk R, White K, Zeidler W (eds) References World Amphipoda Database Accessed through: World Register of Marine Species. http://marin​espec​ies.org/aphia​.php?p=taxde​ Appadoo C, Myers AA (2002) Observations on the tube-building tails​&id=10136​6. Accessed 12 Dec 2017 behaviour of the marine amphipod Cymadusa filosa Savi- Hurley DE (1954) Studies on the New Zealand amphipodan fauna no. gny (Crustacea: Ampithoidae). Journal of Natural History 5. Pleonexes lessoniae a new species of the family Amphithoidae. 37:2151–2164 Trans R Soc N Z 81:619–626

1 3 Marine Biology (2018) 165:184 Page 9 of 9 184

Johnson CR, Mann KH (1986) The importance of plant defence abili- benefts for the giant kelp Macrocystis pyrifera. Mar Ecol Prog ties to the structure of subtidal seaweed communities: the kelp Ser 417:51–158 Laminaria longicruris de la Pylaie survives grazing by the snail Pfster CA, Betcher SP (2018) Climate drivers and animal host use Lacuna vincta (Montagu) at high population densities. J Exp Mar determine kelp performance over decadal scales in the kelp Biol Ecol 97:231–267 Pleurophycus gardneri (Laminariales, Phaeophyceae). J Phycol Jones LG (1971) Studies on selected small herbivorous invertebrates 54:1–11 inhabiting Macrocystis canopies and holdfasts in southern Cali- Poore AGB (2005) Scales of dispersal among hosts in a herbivorous fornia kelp beds. In: North WJ (ed) The biology of giant kelp marine amphipod. Austral Ecol 30:219–228 beds (Macrocystis) in California. Nova Hedwigia (Suppl) 32, pp Poore AGB, Lowry JK (1997) New ampithoid amphipods from Port 343–367 Jackson, New South Wales, Australia (Crustacea: Amphipoda: Kozlov MV, Zvereva EL (2017) Background insect herbivory: impacts, Ampithoidae). Invertebr Taxon 11:897–941 patterns and methodology. In: Cánovas F, Lüttge U, Matyssek R Poore AGB, Hill NA, Sotka EE (2008) Phylogenetic and geographic (eds) Progress in botany, vol 79. Springer, Cham, pp 313–355 variation in host breadth and composition by herbivorous amphi- Krumhansl KA, Jl Lee, Scheibling RE (2011) Grazing damage and pods in the family Ampithoidae. Evolution 62:21–38 encrustation by an invasive bryozoan reduce the ability of kelps Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, to withstand breakage by waves. J Exp Mar Biol Ecol 407:12–18 Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift Lill JT, Marquis RJ (2007) Microhabitat manipulation: ecosystem MA, Dufy JE (2012) Global patterns in the impact of marine engineering by shelter-building insects. In: Cuddington K, Byers herbivores on benthic primary producers. Ecol Lett 15:912–922 JE, Wilson WG, Hastings A (eds) Ecosystem engineers: plants to Poore AGB, Gutow L, Pantoja JF, Tala F, Madariaga DJ, Thiel M protists. Academic Press, New York, pp 107–138 (2014) Major consequences of minor damage: impacts of small Marquis RJ (1996) Plant architecture, sectoriality and plant tolerance grazers on fast-growing kelps. Oecologia 174:789–801 to herbivores. Vegetatio 127:85–97 Reed DC (1987) Factors afecting the production of sporophylls in the Mejaes BA, Poore AGB, Thiel M (2015) Crustaceans inhabiting domi- giant kelp Macrocystis pyrifera (L.) C. Ag. J Exp Mar Biol Ecol ciles excavated from macrophytes and stone. In: Thiel M, Watling 113:61–69 L (eds) The life styles and feeding biology of the Crustacea vol- Schiel DR, Foster MS (2015) The biology and ecology of giant kelp ume II in the natural history of the Crustacea series, vol II. Oxford forests. University of California Press, Oakland University Press, Oxford, pp 118–144 Sliwinski M, Sigmon E (2013) Why do leaf-tying caterpillars abandon Molis M, Enge A, Karsten U (2010) Grazing impact of, and indirect their leaf ties? Peer J 1:e173 interactions between mesograzers associated with kelp (Lami- Stout MJ, Thaler JS, Thomma BPHJ (2006) Plant-mediated interactions naria digitata). J Phycol 46:76–84 between pathogenic microorganisms and herbivorous arthropods. Moore PG, Eastman LB (2015) The tube-dwelling lifestyle in crusta- Annu Rev Entomol 51:663–689 ceans and its relation to feeding. In: Thiel M, Watling L (eds) The Taylor RB (1998) Short-term dynamics of a seaweed epifaunal assem- life styles and feeding biology of the Crustacea volume II in the blage. J Exp Mar Biol Ecol 227:67–82 natural history of the Crustacea series, vol II. Oxford University R Core Team (2017) R: a language and environment for statistical com- Press, Oxford, pp 35–77 puting. R Foundation for Statistical Computing, Vienna, Austria. Muñoz M, Santelices B (1989) Determination of the distribution https​://www.R-proje​ct.org/. Accessed 30 June 2018 and abundance of the limpet Scurria scurra on the stipes of the Tegner MJ, Dayton PK (1987) El Niño efects on southern California kelp Lessonia nigrescens in Central Chile. Mar Ecol Prog Ser kelp forest communities. Adv Ecol Res 17:243–279 54:277–285 Thiel M (2003) Reproductive biology of Limnoria chilensis: another O’Brien JM, Scheibling RE (2016) Nipped in the bud: mesograzer feed- boring peracarid species with extended parental care. J Nat Hist ing preference contributes to kelp decline. Ecology 97:1873–1886 37:1713–1726 Pansch C, Gómez I, Rothäusler E, Véliz K, Thiel M (2008) Species- Toth G, Pavia H (2007) Induced herbivore resistance in seaweeds: a specifc defences strategies of vegetative versus reproductive meta-analysis. J Ecol 95:425–434 blades of the Pacifc kelps Lessonia nigrescens and Macrocystis Zimmerman RC, Kremer JN (1986) In situ growth and chemical com- integrifolia. Mar Biol 155:51–52 position of the giant kelp, Macrocystis pyrifera: response to tem- Peart R, Lörz A (2018) Ampithoidae (Crustacea; Amphipoda) from poral changes in ambient nutrient availability. Mar Ecol Prog Ser New Zealand. Zookeys 733:25–48 27:277–285 Pérez-Matus A, Shima JS (2010) Density- and trait-mediated efects of fish predators on amphipod grazers: potential indirect

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